Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation

Journal of Cell Biology

Volumn 162, Issue 5, 2003, Pages 899-908

  Topol, Lilia ^a   Jiang, Xueyuan ^a,b   Choi, Hosoon ^a   Garrett Beal, Lisa ^a   Carolan, Peter J ^a   Yang, Yingzi ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b NANJING UNIVERSITY   (China)

Author keywords

APC; Cancer; Chondrogenesis; Limb; Siah2

Indexed keywords

APC PROTEIN; BETA CATENIN; BETA TRCP PROTEIN; PROTEIN; SIAH2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CANCER CELL CULTURE; CANCER INHIBITION; CELL CULTURE; COLON CANCER; CONTROLLED STUDY; EMBRYO; GENE; GSK 3 GENE; LIMB DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; WNT GENE; WNT5A GENE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; BETA CATENIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL LINE; CELL LINE, TUMOR; CULTURE TECHNIQUES; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; EMBRYO; EMBRYONIC STRUCTURES; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENES, REPORTER; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; MICE, TRANSGENIC; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; WNT PROTEINS;

ANIMALIA; MAMMALIA;

EID: 0043234811     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200303158     Document Type: Article

References (60)

1. Bienz, M., and H. Clevers. 2003. Armadillo/beta-catenin signals in the nucleus-proof beyond a reasonable doubt? Nat. Cell Biol. 5:179-182.
2. Chan, S.K., and G. Struhl. 2002. Evidence that Armadillo transduces wingless by mediating nuclear export or cytosolic activation of Pangolin. Cell. 111:265-280.
3. Chen, R.H., W.V. Ding, and F. McCormick. 2000. Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J. Biol. Chem. 275:17894-17899.
4. Crabtree, G.R., and E.N. Olson. 2002. NFAT signaling: choreographing the social lives of cells. Cell. 109(Suppl):S67-S79.
5. DasGupta, R., and E. Fuchs. 1999. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 126:4557-4568.
6. Frew, I.J., R.A. Dickins, A.R. Cuddihy, M. Del Rosario, C. Reinhard, M.J. O'Connell, and D.D. Bowtell. 2002. Normal p53 function in primary cells deficient for Siah genes. Mol. Cell. Biol. 22:8155-8164.
7. Habas, R., Y. Kato, and X. He. 2001. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell. 107:843-854.
8. Hartmann, C., and C.J. Tabin. 2001. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell. 104:341-351.
9. Hu, G., and E.R. Fearon. 1999. Siah-1 N-terminal RING domain is required for proteolysis function, and C-terminal sequences regulate oligomerization and binding to target proteins. Mol. Cell. Biol. 19:724-732.
10. Huelsken, J., and W. Birchmeier. 2001. New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11:547-553.
11. Hughes, S.H., J.J. Greenhouse, C.J. Petropoulos, and P. Sutrave. 1987. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61:3004-3012.
12. Ishitani, T., S. Kishida, J. Hyodo-Miura, N. Ueno, J. Yasuda, M. Waterman, H. Shibuya, R.T. Moon, J. Ninomiya-Tsuji, and K. Matsumoto. 2003. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol. Cell. Biol. 23:131-139.
13. Jho, E.H., T. Zhang, C. Domon, C.K. Joo, J.N. Freund, and F. Costantini. 2002. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22:1172-1183.
14. Klein, P.S., and D.A. Melton. 1996. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA. 93:8455-8459.
15. Korinek, V., N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 275:1784-1787.
16. Kuhl, M., L.C. Sheldahl, C.C. Malbon, and R.T. Moon. 2000a. Ca(2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275:12701-12711.
17. 2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16:279-283.
18. Lee, C.S., L.A. Buttitta, N.R. May, A. Kispert, and C.M. Fan. 2000. SHH-N upregulates Sfrp2 to mediate its competitive interaction with WNT1 and WNT4 in the somitic mesoderm. Development. 127:109-118.
19. Lee, K., B. Lanske, A.C. Karaplis, J.D. Deeds, H. Kohno, R.A. Nissenson, H.M. Kronenberg, and G.V. Segte. 1996. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology. 137:5109-5118.
20. Lescher, B., B. Haenig, and A. Kispett. 1998. sFRP-2 is a target of the Wnt-4 signaling pathway in the developing metanephric kidney. Dev. Dyn. 213:440-451.
21. Lickert, H., A. Kispert, S. Kutsch, and R. Kemler. 2001. Expression patterns of Wnt genes in mouse gut development. Mech. Dev. 105:181-184.
22. Liu, J., J. Stevens, C.A. Rote, H.J. Yost, Y. Hu, K.L. Neufeld, R.L. White, and N. Matsunami. 2001. Siah-1 mediates a novel beta-catenin degradation pathway linking p53 to the adenomatous polyposis coli protein. Mol. Cell. 7:927-936.
23. Matsuzawa, S.I., and J.C. Reed. 2001. Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol. Cell. 7:915-926.
24. Meng, L., R. Mohan, B.H. Kwok, M. Elofsson, N. Sin, and C.M. Crews. 1999. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc. Natl. Acad. Sci. USA. 96:10403-10408.
25. Moon, R.T., B. Bowerman, M. Boutros, and N. Perrimon. 2002. The promise and perils of Wnt signaling through beta-catenin. Science. 296:1644-1646.
26. Niehrs, C. 2001. Developmental biology. Solving a sticky problem. Nature. 413:787-788.
27. Olson, D.J., and D.M. Gibo. 1998. Antisense wnt-5a mimics wnt-1-mediated C57MG mammary epithelial cell transformation. Exp. Cell Res. 241:134-141.
28. Parr, B.A., M.J. Shea, G. Vassileva, and A.P. McMahon. 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development. 119:247-261.
29. Peifer, M., and P. Polakis. 2000. Wnt signaling in oncogenesis and embryogenesis-a look outside the nucleus. Science. 287:1606-1609.
30. Pinson, K.I., J. Brennan, S. Monkley, B.J. Avery, and W.C. Skarnes. 2000. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature. 407:535-538.
31. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 273:28424-28429.
32. Rossi, F., H.E. MacLean, W. Yuan, R.O. Francis, E. Semenova, C.S. Lin, H.M. Kronenberg, and D. Cobrinik. 2002. p107 and p130 Coordinately regulate proliferation, Cbfa1 expression, and hypertrophic differentiation during endochondral bone development. Dev. Biol. 247:271-285.
33. Rudnicki, J.A., and A.M. Brown. 1997. Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Dev. Biol. 185:104-118.
34. Ryu, J.H., S.J. Kim, S.H. Kim, C.D. Oh, S.G. Hwang, C.H. Chun, S.H. Oh, J.K. Seong, T.L. Huh, and J.S. Chun. 2002. Regulation of the chondtocyte phenotype by beta-catenin. Development. 129:5541-5550.
35. Saneyoshi, T., S. Kume, Y. Amasaki, and K. Mikoshiba. 2002. The Wnt/calcium pathway activates NF-AT and promotes ventral cell fate in Xenopus embryos. Nature. 417:295-299.
36. Sheidahl, L.C., M. Park, C.C. Malbon, and R.T. Moon. 1999. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9:695-698.
37. Shukunami, C., Y. Ohta, M. Sakuda, and Y. Hiraki. 1998. Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp. Cell Res. 241:1-11.
38. 2+-/calmodulin-dependent protein kinase II. J. Biol. Chem. 276:3719-3722.
39. Solursh, M., C.T. Singley, and R.S. Reitet. 1981. The influence of epithelia on cartilage and loose connective tissue formation by limb mesenchyme cultures. Dev. Biol. 86:471-482.
40. Storm, E.E., and D.M. Kingsley. 1999. GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 209:11-27.
41. Taipale, J., and P.A. Beachy. 2001. The Hedgehog and Wnt signalling pathways in cancer. Nature. 411:349-354.
42. Tetsu, O., and F. McCormick. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 398:422-426.
43. Thorogood, P.V., and J.R. Hinchliffe. 1975. An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J. Embryol. Exp. Morphol. 33:581-606.
44. Thorpe, C.J., A. Schlesinger, and B. Bowerman. 2000. Wnt signalling in Caenorhabditis elegans: regulating repressors and polarizing the cytoskeleton. Trends Cell Biol. 10:10-17.
45. Tolwinski, N.S., M. Wehrli, A. Rives, N. Erdeniz, S. DiNardo, and E. Wieschaus. 2003. Wg/Wnt signal can be transmitted through arrow/LRP5,6 and axin independently of Zw3/Gsk3beta activity. Dev. Cell. 4:407-418.
46. Topol, L.Z., B. Bardot, Q. Zhang, J. Resau, E. Huillard, M. Marx, G. Calothy, and D.G. Blair. 2000. Biosynthesis, post-translation modification, and functional characterization of Drm/Gremlin. J. Biol. Chem. 275:8785-8793.
47. Torres, M.A., J.A. Yang-Snyder, S.M. Purcell, A.A. DeMarais, L.L. McGrew, and R.T. Moon. 1996. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133:1123-1137.
48. van de Wetering, M., R. Cavallo, D. Dooijes, M. van Beest, J. van Es, J. Loureiro, A. Ypma, D. Hursh, T. Jones, A. Bejsovec, et al. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell. 88:789-799.
49. van Noort, M., and H. Clevers. 2002. TCF transcription factors, mediators of Wnt-signaling in development and cancer. Dev. Biol. 244:1-8.
50. Wehrli, M., S.T. Dougan, K. Caldwell, L. O'Keefe, S. Schwartz, D. Vaizel-Ohayon, E. Schejter, A. Tomlinson, and S. DiNardo. 2000. arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature. 407:527-530.
51. Westfall, T.A., R. Brimeyer, J. Twedt, J. Gladon, A. Olberding, M. Furutani-Seiki, and D.C. Slusarski. 2003. Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/β-catenin activity. J. Cell Biol. 162:889-898.
52. Winklbauer, R., A. Medina, R.K. Swain, and H. Steinbeisser. 2001. Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature. 413:856-860.
53. Wodarz, A., and R. Nusse. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:59-88.
54. Yamaguchi, T.P., A. Bradley, A.P. McMahon, and S. Jones. 1999. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development. 126:1211-1223.
55. Yamanaka, H., T. Moriguchi, N. Masuyama, M. Kusakabe, H. Hanafusa, R. Takada, S. Takada, and E. Nishida. 2002. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3:69-75.
56. Yang, Y., and L. Niswander. 1995. Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteropostetior patterning. Cell. 80:939-947.
57. Yang, Y., P. Guillot, Y. Boyd, M.F. Lyon, and A.P. McMahon. 1998. Evidence that preaxial polydactyly in the Doublefoot mutant is due to ectopic Indian Hedgehog signaling. Development. 125:3123-3132.
58. Zeng, W., K.A. Whatton, Jr., J.A. Mack, K. Wang, M. Gadbaw, K. Suyama, P.S. Klein, and M.P. Scott. 2000. Naked cuticle encodes an inducible antagonist of Wnt signalling. Nature. 403:789-795.
59. Zhao, Q., H. Eberspaecher, V. Lefebvre, and B. De Crombrugghe. 1997. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209:377-386.
60. Zorn, A.M., G.D. Barish, B.O. Williams, P. Lavender, M.W. Klymkowsky, and H.E. Varmus. 1999. Regulation of Wnt signaling by Sox proteins: XSox17 alpha/beta and XSox3 physically interact with beta-catenin. Mol. Cell. 4:487-498.