The Dishevelled-associating protein Daple controls the non-canonical Wnt/Rac pathway and cell motility

Nature Communications

Volumn 3, Issue , 2012, Pages

  Ishida Takagishi, Maki ^a   Enomoto, Atsushi ^a   Asai, Naoya ^a   Ushida, Kaori ^a   Watanabe, Takashi ^a   Hashimoto, Takahiko ^a   Kato, Takuya ^a   Weng, Liang ^a   Matsumoto, Shinji ^b   Asai, Masato ^a   Murakumo, Yoshiki ^a   Kaibuchi, Kozo ^a   Kikuchi, Akira ^b   Takahashi, Masahide ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DAPLE PROTEIN; DISHEVELLED PROTEIN; PROTEIN; PROTEIN KINASE C LAMBDA; RAC PROTEIN; UNCLASSIFIED DRUG; WNT5A PROTEIN; CARRIER PROTEIN; DAPLE PROTEIN, MOUSE; DISHEVELLED PROTEINS; PHOSPHOPROTEIN; PROTEIN KINASE C; SIGNAL TRANSDUCING ADAPTOR PROTEIN; WNT PROTEIN; WNT5A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL MOTILITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTERNALIZATION; LAMELLIPODIUM; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL LINE; CELL MOTION; GENETICS; IMMUNOPRECIPITATION; KERATINOCYTE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROTEIN BINDING; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KERATINOCYTES; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN KINASE C; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84866356918     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1861     Document Type: Article

References (50)

1. Wharton, K. A. Jr. Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev. Biol. 253, 1-17 (2003). (Pubitemid 36068000)
2. Habas, R. & Dawid, I. B. Dishevelled and Wnt signaling: is the nucleus the final frontier? J. Biol. 4, 2 (2005).
3. Gao, C. & Chen, Y. G. Dishevelled: the hub of Wnt signaling. Cell. Signal. 22, 717-727 (2010).
4. Zeng, X. et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135, 367-375 (2008). (Pubitemid 351228428)
5. Willert, K. & Nusse, R. Beta-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95-102 (1998). (Pubitemid 28122147)
6. Clevers, H. Wnt/β-Catenin signaling in development and disease. Cell 127, 469-480 (2006).
7. MacDonald, B. T., Tamai, K. & He, X. Wnt/b-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26 (2009).
8. Habas, R., Kato, Y. & He, X. Wnt/Frizzled activation of Rho regulates Vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107, 843-854 (2001). (Pubitemid 34084976)
9. Wallingford, J. B. & Habas, R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132, 4421-4436 (2005). (Pubitemid 41632222)
10. Veeman, M. T., Axelrod, J. D. & Moon, R. T. A second canon: functions and mechanisms of β-catenin-independent Wnt signalling. Dev. Cell 5, 367-377 (2003). (Pubitemid 37107667)
11. Wallingford, J. B., Fraser, S. E. & Harland, R. M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2, 695-706 (2002). (Pubitemid 34657140)
12. De Calisto, J., Araya, C., Marchant, L., Riaz, C. F. & Mayor, R. Essential role of non-canonical Wnt signalling in neural crest migration. Development 132, 2587-2597 (2005). (Pubitemid 40883257)
13. Dabdoub, A. et al. Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130, 2375-2384 (2003). (Pubitemid 36722389)
14. Pandur, P., Läsche, M., Eisenberg, L. M. & Kühl, M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 8, 636-641 (2002).
15. Olson, D. J. & Gibo, D. M. Antisense wnt-5a mimics wnt-1-mediated C57MG mammary epithelial cell transformation. Exp. Cell Res. 241, 134-141 (1998). (Pubitemid 28366587)
16. Weeraratna, A. T. et al. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1, 279-288 (2002). (Pubitemid 41039152)
17. Kurayoshi, M. et al. Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 66, 10439-10448 (2006). (Pubitemid 44799765)
18. Kato, M. WNT/PCP signaling pathway and human cancer. Oncol. Rep. 14, 1583-1588 (2005).
19. Eaton, S., Wepf, R. & Simons, K. Roles for Racl and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135, 1277-1289 (1996). (Pubitemid 27014599)
20. Strutt, D. I., Weber, U. & Mlodzik, M. The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295 (1997). (Pubitemid 27220765)
21. Boutros, M., Paricio, N., Strutt, D. I. & Mlodzik, M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118 (1998). (Pubitemid 28347474)
22. Schlessinger, K., Hall, A. & Tolwinski, N. Wnt signaling pathways meet Rho GTPases. Genes Dev. 23, 265-277 (2009).
23. Habas, R., Dawid, I. B. & He, X. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17, 295-309 (2003). (Pubitemid 36105900)
24. Rosso, S. B., Sussman, D., Wynshaw-Boris, A. & Salinas, P. C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 8, 34-42 (2005). (Pubitemid 41236729)
25. Sato, A., Yamamoto, H., Sakane, H., Koyama, H. & Kikuchi, A. Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 29, 41-54 (2010).
26. Zhang, X. et al. Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat. Cell Biol. 9, 743-754 (2007). (Pubitemid 47019461)
27. Suzuki, A. & Ohno, S. The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119, 979-987 (2006).
28. Etienne-Manneville, S. & Hall, A. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 15, 67-72 (2003). (Pubitemid 36044717)
29. Nishimura, T. et al. PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat. Cell Biol. 7, 270-277 (2005). (Pubitemid 40331128)
30. Oshita, A. et al. Identification and characterization of a novel Dvl-binding protein that suppresses Wnt signalling pathway. Genes Cells 8, 1005-1017 (2003). (Pubitemid 38072276)
31. Kobayashi, H. et al. Novel Daple-like protein positively regulates both the Wnt/β-catenin pathway and the Wnt/JNK pathway in Xenopus. Mech. Dev. 122, 1138-1153 (2005). (Pubitemid 41262430)
32. Tahinci, E. & Symes, K. Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. Dev. Biol. 259, 318-335 (2003). (Pubitemid 36836148)
33. Levine, R L. et al. KIAA1509 is a novel PDGFRB fusion partner in imatinib-responsive myeloproliferative disease associated with a t(5;14)(q33;q32). Leukemia 1, 27-30 (2005). (Pubitemid 40090071)
34. Enomoto, A. et al. Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9, 389-402 (2005). (Pubitemid 41235808)
35. Enomoto, A., Jiang, P. & Takahashi, M. Girdin, a novel actin-binding protein, and its family of proteins possess versatile functions in the Akt and Wnt signaling pathways. Ann. NY Acad. Sci. 1086, 169-184 (2006). (Pubitemid 47084384)
36. Kitamura, T. et al. Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329-337 (2008). (Pubitemid 351331020)
37. Weng, L., Enomoto, A., Ishida-Takagishi, M., Asai, N. & Takahashi, M. Girding for migratory cues: roles of the Akt substrate Girdin in cancer progression and angiogenesis. Cancer Sci. 101, 836-842 (2010).
38. Wang, Y. et al. Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J. Neurosci. 31, 8109-8122 (2011).
39. Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A. & Collard, J. G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol. 147, 1009-1022 (1999).
40. Qian, D. et al. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306, 121-133 (2007). (Pubitemid 46823929)
41. Wong, H. C. et al. Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of frizzled. Mol. Cell 5, 1251-1260 (2003).
42. Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 5, 1704-1709 (2003). (Pubitemid 37505725)
43. Pankov, R. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793-802 (2005). (Pubitemid 41242111)
44. Labus, M. B., Stirk, C. M., Thompson, W. D. & Melvin, W. T. Expression of Wnt genes in early wound healing. Wound Repair Regen. 6, 58-64 (1998). (Pubitemid 128656991)
45. Okuse, T., Chiba, T., Katsuumi, I. & Imai, K. Differential expression and localization of WNTs in an animal model of skin wound healing. Wound Repair Regen. 13, 491-497 (2005). (Pubitemid 41783167)
46. Topol, L. et al. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J. Cell Biol. 5, 899-908 (2003). (Pubitemid 37087729)
47. Yano, K. Gene expression correlation analysis predicts involvement of high- and low-confidence risk genes in different stages of prostate carcinogenesis. Prostate 70, 1746-1759 (2010).
48. Nakayama, M. et al. Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. Dev. Cell 14, 205-215 (2008). (Pubitemid 351189179)
49. Matsumoto, S., Fumoto, K., Okamoto, T., Kaibuchi, K. & Kikuchi, A. Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J. 29, 1192-1204 (2010).
50. Watanabe, T. et al. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 7, 871-883 (2004). (Pubitemid 39654731)