Insight into the Role of Wnt5a-Induced Signaling in Normal and Cancer Cells

International Review of Cell and Molecular Biology

Volumn 314, Issue , 2015, Pages 117-148

  Endo, Mitsuharu ^a   Nishita, Michiru ^a   Fujii, Masanori ^a   Minami, Yasuhiro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer progression; Cell invasion; Convergent extension (CE); Matrix metalloproteinases (MMPs); Planar cell polarity (PCP); Ror1; Ror2; Wnt5a

Indexed keywords

WNT5A PROTEIN; COLLAGENASE; ONCOPROTEIN; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; ROR1 PROTEIN, HUMAN; ROR2 PROTEIN, HUMAN; TUMOR PROTEIN; WNT PROTEIN; WNT5A PROTEIN, HUMAN;

ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER GROWTH; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL CARCINOMA; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; WNT SIGNALING PATHWAY; ANIMAL; CALCIUM SIGNALING; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR INVASION;

MAMMALIA;

ANIMALS; CALCIUM SIGNALING; CELL POLARITY; COLLAGENASES; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS; PROTO-ONCOGENE PROTEINS; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84921614073     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ircmb.2014.10.003     Document Type: Article

References (122)

1. Al-Shawi R., Ashton S.V., Underwood C., Simons J.P. Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev. Genes Evol. 2001, 211:161-171.
2. Anastas J.N., Kulikauskas R.M., Tamir T., Rizos H., Long G.V., von Euw E.M., Yang P.T., Chen H.W., Haydu L., Toroni R.A., Lucero O.M., Chien A.J., Moon R.T. WNT5A enhances resistance of melanoma cells to targeted BRAF inhibitors. J. Clin. Invest. 2014, 124:2877-2890.
3. Andre P., Wang Q., Wang N., Gao B., Schilit A., Halford M.M., Stacker S.A., Zhang X., Yang Y. The Wnt coreceptor Ryk regulates Wnt/planar cell polarity by modulating the degradation of the core planar cell polarity component Vangl2. J. Biol. Chem. 2012, 287:44518-44525.
4. Barald K.F., Kelley M.W. From placode to polarization: new tunes in inner ear development. Development 2004, 131:4119-4130.
5. Barna G., Mihalik R., Timar B., Tombol J., Csende Z., Sebestyen A., Bodor C., Csernus B., Reiniger L., Petak I., Matolcsy A. ROR1 expression is not a unique marker of CLL. Hematol. Oncol. 2011, 29:17-21.
6. Barrallo-Gimeno A., Nieto M.A. The snail genes as inducers of cell movementand survival: implications in development and cancer. Development 2005, 132:3151-3161.
7. Baskar S., Kwong K.Y., Hofer T., Levy J.M., Kennedy M.G., Lee E., Staudt L.M., Wilson W.H., Wiestner A., Rader C. Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin. Cancer Res. 2008, 14:396-404.
8. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
9. Bean J., Brennan C., Shih J.Y., Riely G., Viale A., Wang L., Chitale D., Motoi N., Szoke J., Broderick S., Balak M., Chang W.C., Yu C.J., Gazdar A., Pass H., Rusch V., Gerald W., Huang S.F., Yang P.C., Miller V., Ladanyi M., Yang C.H., Pao W. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc. Natl. Acad. Sci. USA 2007, 104:20932-20937.
10. Bicocca V.T., Chang B.H., Masouleh B.K., Muschen M., Loriaux M.M., Druker B.J., Tyner J.W. Crosstalk between ROR1 and the pre-B cell receptor promotes survival of t(1;19) acute lymphoblastic leukemia. Cancer Cell 2012, 22:656-667.
11. Cacalano G., Farinas I., Wang L.C., Hagler K., Forgie A., Moore M., Armanini M., Phillips H., Ryan A.M., Reichardt L.F., Hynes M., Davies A., Rosenthal A. GFRα1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 1998, 21:53-62.
12. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
13. Chen P., Johnson J.E., Zoghbi H.Y., Segil N. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 2002, 129:2495-2505.
14. Copp A.J., Greene N.D. Genetics and development of neural tube defects. J. Pathol. 2010, 220:217-230.
15. Cui B., Zhang S., Chen L., Yu J., Widhopf G.F., Fecteau J.F., Rassenti L.Z., Kipps T.J. Targeting ROR1 inhibits epithelial-mesenchymal transition and metastasis. Cancer Res. 2013, 73:3649-3660.
16. Daneshmanesh A.H., Mikaelsson E., Jeddi-Tehrani M., Bayat A.A., Ghods R., Ostadkarampour M., Akhondi M., Lagercrantz S., Larsson C., Osterborg A., Shokri F., Mellstedt H., Rabbani H. Ror1, a cell surface receptor tyrosine kinase is expressed in chronic lymphocytic leukemia and may serve as a putative target for therapy. Int. J. Cancer 2008, 123:1190-1195.
17. Delaunay D., Cortay V., Patti D., Knoblauch K., Dehay C. Mitotic spindle asymmetry: a Wnt/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell rep. 2014, 6:400-414.
18. Dissanayake S.K., Wade M., Johnson C.E., O'Connell M.P., Leotlela P.D., French A.D., Shah K.V., Hewitt K.J., Rosenthal D.T., Indig F.E., Jiang Y., Nickoloff B.J., Taub D.D., Trent J.M., Moon R.T., Bittner M., Weeraratna A.T. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J. Biol. Chem. 2007, 282:17259-17271.
19. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
20. Elul T., Keller R. Monopolar protrusive activity: a new morphogenic cell behavior in the neural plate dependent on vertical interactions with the mesoderm in Xenopus. Dev. Biol. 2000, 224:3-19.
21. Endo M., Doi R., Nishita M., Minami Y. Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J. Cell Sci. 2012, 125:2017-2029.
22. Engelman J.A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Park J.O., Lindeman N., Gale C.M., Zhao X., Christensen J., Kosaka T., Holmes A.J., Rogers A.M., Cappuzzo F., Mok T., Lee C., Johnson B.E., Cantley L.C., Janne P.A. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
23. Enomoto H., Araki T., Jackman A., Heuckeroth R.O., Snider W.D., Johnson E.M., Milbrandt J. GFRα1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 1998, 21:317-324.
24. Enomoto M., Hayakawa S., Itsukushima S., Ren D.Y., Matsuo M., Tamada K., Oneyama C., Okada M., Takumi T., Nishita M., Minami Y. Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 2009, 28:3197-3208.
25. Etheridge S.L., Ray S., Li S., Hamblet N.S., Lijam N., Tsang M., Greer J., Kardos N., Wang J., Sussman D.J., Chen P., Wynshaw-Boris A. Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genet. 2008, 4:e1000259.
26. Feike A.C., Rachor K., Gentzel M., Schambony A. Wnt5a/Ror2-induced upregulation of xPAPC requires xShcA. Biochem. Biophys. Res. Commun. 2010, 400:500-506.
27. Forrester W.C., Dell M., Perens E., Garriga G. A C. elegans Ror receptortyrosine kinase regulates cell motility and asymmetric cell division. Nature 1999, 400:881-885.
28. Fukuda T., Chen L., Endo T., Tang L., Lu D., Castro J.E., Widhopf G.F., Rassenti L.Z., Cantwell M.J., Prussak C.E., Carson D.A., Kipps T.J. Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc. Natl. Acad. Sci. USA 2008, 105:3047-3052.
29. Gao B., Song H., Bishop K., Elliot G., Garrett L., English M.A., Andre P., Robinson J., Sood R., Minami Y., Economides A.N., Yang Y. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 2011, 20:163-176.
30. Gentile A., Lazzari L., Benvenuti S., Trusolino L., Comoglio P.M. Ror1 isapseudokinase that is crucial for Met-driven tumorigenesis. Cancer Res. 2011, 71:3132-3141.
31. Gentile A., Lazzari L., Benvenuti S., Trusolino L., Comoglio P.M. The ROR1 pseudokinase diversifies signaling outputs in MET-addicted cancer cells. Int. J. Cancer 2014, 135:2305-2316.
32. Grumolato L., Liu G., Mong P., Mudbhary R., Biswas R., Arroyave R., Vijayakumar S., Economides A.N., Aaronson S.A. Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 2010, 24:2517-2530.
33. He F., Xiong W., Yu X., Espinoza-Lewis R., Liu C., Gu S., Nishita M., Suzuki K., Yamada G., Minami Y., Chen Y. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development 2008, 135:3871-3879.
34. Hikasa H., Shibata M., Hiratani I., Taira M. The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 2002, 129:5227-5239.
35. Ho H.Y., Susman M.W., Bikoff J.B., Ryu Y.K., Jonas A.M., Hu L., Kuruvilla R., Greenberg M.E. Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc. Natl. Acad. Sci. USA 2012, 109:4044-4051.
36. Hojjat-Farsangi M., Khan A.S., Daneshmanesh A.H., Moshfegh A., Sandin A., Mansouri L., Palma M., Lundin J., Osterborg A., Mellstedt H. The tyrosine kinase receptor ROR1 is constitutively phosphorylated in chronic lymphocytic leukemia (CLL) cells. PLoS One 2013, 8:e78339.
37. Hoshi M., Batourina E., Mendelsohn C., Jain S. Novel mechanisms of early upper and lower urinary tract patterning regulated by RetY1015 docking tyrosine in mice. Development 2012, 139:2405-2415.
38. Ishida-Takagishi M., Enomoto A., Asai N., Ushida K., Watanabe T., Hashimoto T., Kato T., Weng L., Matsumoto S., Asai M., Murakumo Y., Kaibuchi K., Kikuchi A., Takahashi M. The Dishevelled-associating protein Daple controls the non-canonical Wnt/Rac pathway and cell motility. Nat. Commun. 2012, 3:859.
39. Jessen J.R., Topczewski J., Bingham S., Sepich D.S., Marlow F., Chandrasekhar A., Solnica-Krezel L. Zebrafish trilobite identifies new roles for strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 2002, 4:610-615.
40. Jiang W., Crossman D.K., Mitchell E.H., Sohn P., Crowley M.R., Serra R. WNT5A inhibits metastasis and alters splicing of Cd44 in breast cancer cells. PLoS One 2013, 8:e58329.
41. Jiao Y., Feng X., Zhan Y., Wang R., Zheng S., Liu W., Zeng X. Matrix metalloproteinase-2 promotes alphavbeta3 integrin-mediated adhesion and migration of human melanoma cells by cleaving fibronectin. PLoS One 2012, 7:e41591.
42. Jonsson M., Dejmek J., Bendahl P.O., Andersson T. Loss of Wnt-5a protein is associated with early relapse in invasive ductal breast carcinomas. Cancer Res. 2002, 62:409-416.
43. Keller R., Davidson L., Edlund A., Elul T., Ezin M., Shook D., Skoglund P. Mechanisms of convergence and extension by cell intercalation. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2000, 355:897-922.
44. Kikuchi A., Yamamoto H. Tumor formation due to abnormalities in the beta-catenin-independent pathway of Wnt signaling. Cancer Sci. 2008, 99:202-208.
45. Kobayashi S., Boggon T.J., Dayaram T., Janne P.A., Kocher O., Meyerson M., Johnson B.E., Eck M.J., Tenen D.G., Halmos B. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 2005, 352:786-792.
46. Kohn A.D., Moon R.T. Wnt and calcium signaling: β-catenin-independent pathways. Cell Calcium 2005, 38:439-446.
47. Kreso A., Dick J.E. Evolution of the cancer stem cell model. Cell Stem Cell 2014, 14:275-291.
48. Kurrey N.K., K A., Bapat S.A. Snail and slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol. 2005, 97:155-165.
49. Laird D.J., Altshuler-Keylin S., Kissner M.D., Zhou X., Anderson K.V. Ror2 enhances polarity and directional migration of primordial germ cells. PLoS Genet. 2011, 7:e1002428.
50. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 2006, 172:973-981.
51. Liu Y., Rubin B., Bodine P.V., Billiard J. Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J. Cell. Biochem. 2008, 105:497-502.
52. Macheda M.L., Sun W.W., Kugathasan K., Hogan B.M., Bower N.I., Halford M.M., Zhang Y.F., Jacques B.E., Lieschke G.J., Dabdoub A., Stacker S.A. The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. J. Biol. Chem. 2012, 287:29312-29323.
53. MacLeod R.J., Hayes M., Pacheco I. Wnt5a secretion stimulated by the extracellular calcium-sensing receptor inhibits defective Wnt signaling in colon cancer cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G403-G411.
54. Maeda K., Kobayashi Y., Udagawa N., Uehara S., Ishihara A., Mizoguchi T., Kikuchi Y., Takada I., Kato S., Kani S., Nishita M., Marumo K., Martin T.J., Minami Y., Takahashi N. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat. Med. 2012, 18:405-412.
55. Matsuda T., Nomi M., Ikeya M., Kani S., Oishi I., Terashima T., Takada S., Minami Y. Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech. Dev. 2001, 105:153-156.
56. Mericskay M., Kitajewski J., Sassoon D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 2004, 131:2061-2072.
57. Mikels A.J., Nusse R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 2006, 4:e115.
58. Miyoshi A., Kitajima Y., Sumi K., Sato K., Hagiwara A., Koga Y., Miyazaki K. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br. J. Cancer 2004, 90:1265-1273.
59. Moon R.T., Campbell R.M., Christian J.L., McGrew L.L., Shih J., Fraser S. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 1993, 119:97-111.
60. Moore M.W., Klein R.D., Farinas I., Sauer H., Armanini M., Phillips H., Reichardt L.F., Ryan A.M., Carver-Moore K., Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature 1996, 382:76-79.
61. Nishita M., Itsukushima S., Nomachi A., Endo M., Wang Z., Inaba D., Qiao S., Takada S., Kikuchi A., Minami Y. Ror2/Frizzled complex mediates Wnt5a-induced AP-1 activation by regulating dishevelled polymerization. Mol. Cell. Biol. 2010, 30:3610-3619.
62. Nishita M., Qiao S., Miyamoto M., Okinaka Y., Yamada M., Hashimoto R., Iijima K., Otani H., Hartmann C., Nishinakamura R., Minami Y. Role of Wnt5a-Ror2 signaling in morphogenesis of the metanephric mesenchyme during ureteric budding. Mol. Cell. Biol. 2014, 34:3096-3105.
63. Nishita M., Yoo S.K., Nomachi A., Kani S., Sougawa N., Ohta Y., Takada S., Kikuchi A., Minami Y. Filopodia formation mediated by receptor tyrosinekinase Ror2 is required for Wnt5a-induced cell migration. J. Cell Biol. 2006, 175:555-562.
64. Nomachi A., Nishita M., Inaba D., Enomoto M., Hamasaki M., Minami Y. 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. 2008, 283:27973-27981.
65. Nomi M., Oishi I., Kani S., Suzuki H., Matsuda T., Yoda A., Kitamura M., Itoh K., Takeuchi S., Takeda K., Akira S., Ikeya M., Takada S., Minami Y. Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice: redundant and pleiotropic functions of mRor1 and mRor2 receptor tyrosine kinases. Mol. Cell. Biol. 2001, 21:8329-8335.
66. O'Connell M.P., Fiori J.L., Baugher K.M., Indig F.E., French A.D., Camilli T.C., Frank B.P., Earley R., Hoek K.S., Hasskamp J.H., Elias E.G., Taub D.D., Bernier M., Weeraratna A.T. Wnt5A activates the calpain-mediated cleavage of filamin A. J. Invest. Dermatol. 2009, 129:1782-1789.
67. O'Connell M.P., Fiori J.L., Xu M., Carter A.D., Frank B.P., Camilli T.C., French A.D., Dissanayake S.K., Indig F.E., Bernier M., Taub D.D., Hewitt S.M., Weeraratna A.T. The orphan tyrosine kinase receptor, ROR2, mediates Wnt5A signaling in metastatic melanoma. Oncogene 2010, 29:34-44.
68. Oishi I., Sugiyama S., Liu Z.J., Yamamura H., Nishida Y., Minami Y. A novel Drosophila receptor tyrosine kinase expressed specifically in the nervous system. Unique structural features and implication in developmental signaling. J. Biol. Chem. 1997, 272:11916-11923.
69. Oishi I., Suzuki H., Onishi N., Takada R., Kani S., Ohkawara B., Koshida I., Suzuki K., Yamada G., Schwabe G.C., Mundlos S., Shibuya H., Takada S., Minami Y. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 2003, 8:645-654.
70. Oishi I., Takeuchi S., Hashimoto R., Nagabukuro A., Ueda T., Liu Z.J., Hatta T., Akira S., Matsuda Y., Yamamura H., Otani H., Minami Y. Spatio-temporally regulated expression of receptor tyrosine kinases, mRor1, mRor2, during mousedevelopment: implications in development and function of the nervous system. Genes Cells 1999, 4:41-56.
71. Oskarsson T., Batlle E., Massague J. Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell 2014, 14:306-321.
72. Pao W., Miller V.A., Politi K.A., Riely G.J., Somwar R., Zakowski M.F., Kris M.G., Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005, 2:e73.
73. Pichel J.G., Shen L., Sheng H.Z., Granholm A.C., Drago J., Grinberg A., Lee E.J., Huang S.P., Saarma M., Hoffer B.J., Sariola H., Westphal H. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996, 382:73-76.
74. Prasad C.P., Chaurasiya S.K., Axelsson L., Andersson T. WNT-5A triggers Cdc42 activation leading to an ERK1/2 dependent decrease in MMP9 activity and invasive migration of breast cancer cells. Mol. Oncol. 2013, 7:870-883.
75. Qian D., Jones C., Rzadzinska A., Mark S., Zhang X., Steel K.P., Dai X., Chen P. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 2007, 306:121-133.
76. Ren D., Minami Y., Nishita M. Critical role of Wnt5a-Ror2 signaling in motility and invasiveness of carcinoma cells following snail-mediated epithelial-mesenchymal transition. Genes Cells 2011, 16:304-315.
77. Roarty K., Serra R. Wnt5a is required for proper mammary gland development and TGF-beta-mediated inhibition of ductal growth. Development 2007, 134:3929-3939.
78. Safholm A., Leandersson K., Dejmek J., Nielsen C.K., Villoutreix B.O., Andersson T. A formylated hexapeptide ligand mimics the ability of Wnt-5a to impair migration of human breast epithelial cells. J. Biol. Chem. 2006, 281:2740-2749.
79. Safholm A., Tuomela J., Rosenkvist J., Dejmek J., Harkonen P., Andersson T. The Wnt-5a-derived hexapeptide Foxy-5 inhibits breast cancer metastasis in vivo by targeting cell motility. Clin. Cancer Res. 2008, 14:6556-6563.
80. Sanchez M.P., Silos-Santiago I., Frisen J., He B., Lira S.A., Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 1996, 382:70-73.
81. Sato A., Yamamoto H., Sakane H., Koyama H., Kikuchi A. Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 2010, 29:41-54.
82. Saxen L. Organogenesis of the Kidney 1987, Cambridge University Press, Cambridge.
83. Schambony A., Wedlich D. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell 2007, 12:779-792.
84. Schlessinger K., McManus E.J., Hall A. Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J. Cell Biol. 2007, 178:355-361.
85. Schuchardt A., D'Agati V., Larsson-Blomberg L., Costantini F., Pachnis V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994, 367:380-383.
86. Schwabe G.C., Trepczik B., Suring K., Brieske N., Tucker A.S., Sharpe P.T., Minami Y., Mundlos S. Ror2 knockout mouse as a model for the developmentalpathology of autosomal recessive Robinow syndrome. Dev. Dyn. 2004, 229:400-410.
87. Shabani M., Asgarian-Omran H., Jeddi-Tehrani M., Vossough P., Faranoush M., Sharifian R.A., Toughe G.R., Kordmahin M., Khoshnoodi J., Roohi A., Tavoosi N., Mellstedt H., Rabbani H., Shokri F. Overexpression of orphan receptor tyrosine kinase Ror1 as a putative tumor-associated antigen in Iranian patients with acute lymphoblastic leukemia. Tumour Biol. 2007, 28:318-326.
88. Shih J., Keller R. Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 1992, 116:901-914.
89. Shindo A., Wallingford J.B. PCP and septins compartmentalize cortical actomyosin to direct collective cell movement. Science 2014, 343:649-652.
90. Takeuchi M., Nakabayashi J., Sakaguchi T., Yamamoto T.S., Takahashi H., Takeda H., Ueno N. The prickle-related gene in vertebrates is essential for gastrulation cell movements. Curr. Biol. 2003, 13:674-679.
91. 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. Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 2000, 5:71-78.
92. Taki M., Kamata N., Yokoyama K., Fujimoto R., Tsutsumi S., Nagayama M. Down-regulation of Wnt-4 and up-regulation of Wnt-5a expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Cancer Sci. 2003, 94:593-597.
93. Tam P.P., Tan S.S. The somitogenetic potential of cells in the primitive streak and the tail bud of the organogenesis-stage mouse embryo. Development 1992, 115:703-715.
94. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
95. Turke A.B., Zejnullahu K., Wu Y.L., Song Y., Dias-Santagata D., Lifshits E., Toschi L., Rogers A., Mok T., Sequist L., Lindeman N.I., Murphy C., Akhavanfard S., Yeap B.Y., Xiao Y., Capelletti M., Iafrate A.J., Lee C., Christensen J.G., Engelman J.A., Janne P.A. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010, 17:77-88.
96. Unterseher F., Hefele J.A., Giehl K., De Robertis E.M., Wedlich D., Schambony A. Paraxial protocadherin coordinates cell polarity during convergent extension via Rho A and JNK. EMBO J. 2004, 23:3259-3269.
97. van Amerongen R., Mikels A., Nusse R. Alternative wnt signaling is initiated by distinct receptors. Sci. Signal. 2008, 1:re9.
98. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 136:3205-3214.
99. Veeman M.T., Axelrod J.D., Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 2003, 5:367-377.
100. Vladar E.K., Antic D., Axelrod J.D. Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb. Perspect. Biol. 2009, 1:a002964.
101. Wallingford J.B., Harland R.M. Xenopus dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development 2001, 128:2581-2592.
102. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 2000, 405:81-85.
103. Wang Y., Guo N., Nathans J. The role of Frizzled3 and Frizzled6 in neural tubeclosure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci. 2006, 26:2147-2156.
104. Wansleeben C., Meijlink F. The planar cell polarity pathway in vertebrate development. Dev. Dyn. 2011, 240:616-626.
105. Weeraratna A.T., Jiang Y., Hostetter G., Rosenblatt K., Duray P., Bittner M., Trent J.M. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 2002, 1:279-288.
106. Wilson C., Goberdhan D.C., Steller H. Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trk-related receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 1993, 90:7109-7113.
107. Wilson V., Beddington R.S. Cell fate and morphogenetic movement in the late mouse primitive streak. Mech. Dev. 1996, 55:79-89.
108. Wodarz A., Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 1998, 14:59-88.
109. Wright T.M., Brannon A.R., Gordan J.D., Mikels A.J., Mitchell C., Chen S., Espinosa I., van de Rijn M., Pruthi R., Wallen E., Edwards L., Nusse R., Rathmell W.K. Ror2, a developmentally regulated kinase, promotes tumor growth potential in renal cell carcinoma. Oncogene 2009, 28:2513-2523.
110. Wu G., Huang X., Hua Y., Mu D. Roles of planar cell polarity pathways in the development of neural tube defects. J. Biomed. Sci. 2011, 18:66.
111. Xu X., Wang Y., Chen Z., Sternlicht M.D., Hidalgo M., Steffensen B. Matrix metalloproteinase-2 contributes to cancer cell migration on collagen. Cancer Res. 2005, 65:130-136.
112. Yamagata K., Li X., Ikegaki S., Oneyama C., Okada M., Nishita M., Minami Y. Dissection of Wnt5a-Ror2 signaling leading to matrix metalloproteinase (MMP-13). Expr. J. Biol. Chem. 2012, 287:1588-1599.
113. Yamaguchi T., Yanagisawa K., Sugiyama R., Hosono Y., Shimada Y., Arima C., Kato S., Tomida S., Suzuki M., Osada H., Takahashi T. NKX2-1/TITF1/TTF-1-Induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell 2012, 21:348-361.
114. Yamaguchi T.P., Bradley A., McMahon A.P., Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999, 126:1211-1223.
115. Yamamoto H., Oue N., Sato A., Hasegawa Y., Yamamoto H., Matsubara A., Yasui W., Kikuchi A. Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 2010, 29:2036-2046.
116. Yamamoto S., Nishimura O., Misaki K., Nishita M., Minami Y., Yonemura S., Tarui H., Sasaki H. Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev. Cell 2008, 15:23-36.
117. Yamanaka H., Moriguchi T., Masuyama N., Kusakabe M., Hanafusa H., Takada R., Takada S., Nishida E. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 2002, 3:69-75.
118. Yano S., Wang W., Li Q., Matsumoto K., Sakurama H., Nakamura T., Ogino H., Kakiuchi S., Hanibuchi M., Nishioka Y., Uehara H., Mitsudomi T., Yatabe Y., Nakamura T., Sone S. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res. 2008, 68:9479-9487.
119. Ying J., Li H., Yu J., Ng K.M., Poon F.F., Wong S.C., Chan A.T., Sung J.J., Tao Q. WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/β-catenin signaling, and is frequently methylated in colorectal cancer. Clin. Cancer Res. 2008, 14:55-61.
120. Zallen J.A. Planar polarity and tissue morphogenesis. Cell 2007, 129:1051-1063.
121. Zhang S., Chen L., Cui B., Chuang H.Y., Yu J., Wang-Rodriguez J., Tang L., Chen G., Basak G.W., Kipps T.J. ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PLoS One 2012, 7:e31127.
122. Zhang X., Zhu J., Yang G.Y., Wang Q.J., Qian L., Chen Y.M., Chen F., Tao Y., Hu H.S., Wang T., Luo Z.G. Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat. Cell Biol. 2007, 9:743-754.