Induced Wnt5a expression perturbs embryonic outgrowth and intestinal elongation, but is well-tolerated in adult mice

Developmental Biology

Volumn 369, Issue 1, 2012, Pages 91-100

  Bakker, Elvira R M ^a   Raghoebir, Lalini ^a   Franken, Patrick F ^a   Helvensteijn, Werner ^a   van Gurp, Léon ^b   Meijlink, Frits ^b   van der Valk, Martin A ^c   Rottier, Robbert J ^a   Kuipers, Ernst J ^a   van Veelen, Wendy ^a   Smits, Ron ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Development; Homeostasis; Intestine; Mouse model; Ror2; Wnt5a

Indexed keywords

GROWTH FACTOR RECEPTOR; ROR2 PROTEIN; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE SEVERITY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FACE MALFORMATION; GASTROINTESTINAL MALFORMATION; GENE SILENCING; HOMEOSTASIS; IN VIVO STUDY; INTESTINE MALFORMATION; KNOCKOUT MOUSE; LIMB MALFORMATION; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; TAIL;

MUS; MUS MUSCULUS;

EID: 84864375057     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.06.007     Document Type: Article

References (38)

1. Acconcia F., Sigismund S., Polo S. Ubiquitin in trafficking: the network at work. Exp. Cell. Res. 2009, 315:1610-1618.
2. Akbarzadeh S., Wheldon L.M., Sweet S.M., Talma S., Mardakheh F.K., Heath J.K. The deleted in brachydactyly B domain of Ror2 is required for receptor activation by recruitment of Src. PLoS One 2008, 3:e1873.
3. Albuquerque C., Bakker E.R., van Veelen W., Smits R. Colorectal cancers choosing sides. Biochim. Biophys. Acta 2011, 1816:219-231.
4. Blumenthal A., Ehlers S., Lauber J., Buer J., Lange C., Goldmann T., Heine H., Brandt E., Reiling N. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 2006, 108:965-973.
5. Cervantes S., Yamaguchi T.P., Hebrok M. Wnt5a is essential for intestinal elongation in mice. Dev. Biol. 2009, 326:285-294.
6. Chen W., ten Berge D., Brown J., Ahn S., Hu L.A., Miller W.E., Caron M.G., Barak L.S., Nusse R., Lefkowitz R.J. Dishevelled 2 recruits beta-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 2003, 301:1391-1394.
7. Cheng C.W., Yeh J.C., Fan T.P., Smith S.K., Charnock-Jones D.S. Wnt5a-mediated non-canonical Wnt signalling regulates human endothelial cell proliferation and migration. Biochem. Biophys. Res. Commun. 2008, 365:285-290.
8. DeChiara T.M., Kimble R.B., Poueymirou W.T., Rojas J., Masiakowski P., Valenzuela D.M., Yancopoulos G.D. Ror2, encoding a receptor-like tyrosine kinase, is required for cartilage and growth plate development. Nat. Genet. 2000, 24:271-274.
9. Gavin B.J., McMahon J.A., McMahon A.P. Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development. Genes. Dev. 1990, 4:2319-2332.
10. Green J.L., Kuntz S.G., Sternberg P.W. Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol. 2008, 18:536-544.
11. Gregorieff A., Pinto D., Begthel H., Destree O., Kielman M., Clevers H. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 2005, 129:626-638.
12. Gros J., Hu J.K., Vinegoni C., Feruglio P.F., Weissleder R., Tabin C.J. WNT5A/JNK and FGF/MAPK pathways regulate the cellular events shaping the vertebrate limb bud. Curr. Biol. 2010, 20:1993-2002.
13. 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.
14. 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. U S A 2012, 109:4044-4051.
15. Katsantoni E.Z., Anghelescu N.E., Rottier R., Moerland M., Antoniou M., de Crom R., Grosveld F., Strouboulis J. Ubiquitous expression of the rtTA2S-M2 inducible system in transgenic mice driven by the human hnRNPA2B1/CBX3 CpG island. BMC Dev. Biol. 2007, 7:108.
16. Kikuchi A., Yamamoto H., Sato A., Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. (Oxf). 2012, 204:17-33.
17. Lickert H., Kispert A., Kutsch S., Kemler R. Expression patterns of Wnt genes in mouse gut development. Mech. Dev. 2001, 105:181-184.
18. Mikels A., Minami Y., Nusse R. Ror2 receptor requires tyrosine kinase activity to mediate Wnt5A signaling. J. Biol. Chem. 2009, 284:30167-30176.
19. Mikels A.J., Nusse R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 2006, 4:e115.
20. Nishita M., Enomoto M., Yamagata K., Minami Y. Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 2010, 20:346-354.
21. 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.
22. 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.
23. Oh D.Y., Olefsky J.M. Medicine. Wnt fans the flames in obesity. Science 2010, 329:397-398.
24. Ohkawara B., Glinka A., Niehrs C. Rspo3 binds syndecan 4 and induces Wnt/PCP signaling via clathrin-mediated endocytosis to promote morphogenesis. Dev. Cell 2011, 20:303-314.
25. 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.
26. Ouchi N., Higuchi A., Ohashi K., Oshima Y., Gokce N., Shibata R., Akasaki Y., Shimono A., Walsh K. Sfrp5 is an anti-inflammatory adipokine that modulates metabolic dysfunction in obesity. Science 2010, 329:454-457.
27. Pereira C.P., Bachli E.B., Schoedon G. The wnt pathway: a macrophage effector molecule that triggers inflammation. Curr. Atheroscler. Rep. 2009, 11:236-242.
28. Pukrop T., Binder C. The complex pathways of Wnt 5a in cancer progression. J. Mol. Med. 2008, 86:259-266.
29. Reya T., Clevers H. Wnt signalling in stem cells and cancer. Nature 2005, 434:843-850.
30. Rives A.F., Rochlin K.M., Wehrli M., Schwartz S.L., DiNardo S. Endocytic trafficking of Wingless and its receptors, Arrow and DFrizzled-2, in the Drosophila wing. Dev. Biol. 2006, 293:268-283.
31. 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.
32. Smith K., Bui T.D., Poulsom R., Kaklamanis L., Williams G., Harris A.L. Up-regulation of macrophage wnt gene expression in adenoma-carcinoma progression of human colorectal cancer. B. J. Cancer. 1999, 81:496-502.
33. 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.
34. Terabayashi T., Funato Y., Fukuda M., Miki H. A coated vesicle-associated kinase of 104kDa (CVAK104) induces lysosomal degradation of frizzled 5 (Fzd5). J. Biol. Chem. 2009, 284:26716-26724.
35. van Veelen W., Le N.H., Helvensteijn W., Blonden L., Theeuwes M., Bakker E.R., Franken P.F., van Gurp L., Meijlink F., van der Valk M.A., Kuipers E.J., Fodde R., Smits R. {beta}-catenin tyrosine 654 phosphorylation increases Wnt signalling and intestinal tumorigenesis. Gut 2011, 60:1204-1212.
36. 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.
37. Yamada M., Udagawa J., Matsumoto A., Hashimoto R., Hatta T., Nishita M., Minami Y., Otani H. Ror2 is required for midgut elongation during mouse development. Dev. Dyn. 2010, 239:941-953.
38. 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.