The N- or C-terminal domains of DSH-2 can activate the C. elegans Wnt/β-catenin asymmetry pathway

Developmental Biology

Volumn 328, Issue 2, 2009, Pages 234-244

  King, Ryan S ^a   Maiden, Stephanie L ^a   Hawkins, Nancy C ^b   Kidd III, Ambrose R ^a   Kimble, Judith ^a,c   Hardin, Jeff ^a   Walston, Timothy D ^d  

^a UNIVERSITY OF WISCONSIN   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d TRUMAN STATE UNIVERSITY   (United States)

Author keywords

C. elegans; Dishevelled; Morphogenesis

Indexed keywords

BETA CATENIN; DISHEVELLED 2; T CELL FACTOR PROTEIN; WNT1 PROTEIN;

AMINO TERMINAL SEQUENCE; ANTERIOR POSTERIOR AXIS; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CELL FATE; HUMAN; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSGENE; ZYGOTE;

CAENORHABDITIS ELEGANS;

EID: 63349094541     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.01.017     Document Type: Article

References (77)

1. Axelrod J.D., Miller J.R., Shulman J.M., Moon R.T., and Perrimon N. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12 (1998) 2610-2622
2. Bei Y., et al. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev. Cell 3 (2002) 113-125
3. Bischoff M., and Schnabel R. Global cell sorting is mediated by local cell-cell interactions in the C. elegans embryo. Dev. Biol. 294 (2006) 432-444
4. Boutros M., and Mlodzik M. Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech. Dev. 83 (1999) 27-37
5. Boutros M., Paricio N., Strutt D.I., and Mlodzik M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94 (1998) 109-118
6. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
7. Cadigan K.M., and Nusse R. Wnt signaling: a common theme in animal development. Genes Dev. 11 (1997) 3286-3305
8. Chang W., Lloyd C.E., and Zarkower D. DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad. Mech. Dev. 122 (2005) 781-789
9. Chase D.L., Patikoglou G.A., and Koelle M.R. Two RGS proteins that inhibit Galpha(o) and Galpha(q) signaling in C. elegans neurons require a Gbeta(5)-like subunit for function. Curr. Biol. 11 (2001) 222-231
10. Copp A.J., Greene N.D., and Murdoch J.N. Dishevelled: linking convergent extension with neural tube closure. Trends Neurosci. 26 (2003) 453-455
11. Costa M., Raich W., Agbunag C., Leung B., Hardin J., and Priess J.R. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141 (1998) 297-308
12. Eisenmann D.M. Wnt signaling. In: Community T.C.e.R. (Ed). "WormBook" (2005). http://www.wormbook.org Vol. http://www.wormbook.org
13. Finney M., and Ruvkun G. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63 (1990) 895-905
14. Gu T., Orita S., and Han M. Caenorhabditis elegans SUR-5, a novel but conserved protein, negatively regulates LET-60 Ras activity during vulval induction. Mol. Cell Biol. 18 (1998) 4556-4564
15. Guenther C., and Garriga G. Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates. Development 122 (1996) 3509-3518
16. Hawkins N.C., Ellis G.C., Bowerman B., and Garriga G. MOM-5 frizzled regulates the distribution of DSH-2 to control C. elegans asymmetric neuroblast divisions. Dev. Biol. 284 (2005) 246-259
17. Hawkins, N.C., Garriga, G., and Beh, C.T., (2003). Creating precise GFP fusions in plasmids using yeast homologous recombination. Biotechniques 34, 74-8, 80.
18. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., and Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 (2000) 76-81
19. Herman M. C. elegans POP-1/TCF functions in a canonical Wnt pathway that controls cell migration and in a noncanonical Wnt pathway that controls cell polarity. Development 128 (2001) 581-590
20. Herman M.A., and Wu M. Noncanonical Wnt signaling pathways in C. elegans converge on POP-1/TCF and control cell polarity. Front Biosci. 9 (2004) 1530-1539
21. Hingwing K., Lee S., Nykilchuk L., Walston T., Hardin J., and Hawkins N. CWN-1 functions with DSH-2 to regulate C. elegans asymmetric neuroblast division in a β-catenin independent Wnt pathway. Dev. Biol. 328 (2009) 245-256
22. Huang S., Shetty P., Robertson S.M., and Lin R. Binary cell fate specification during C. elegans embryogenesis driven by reiterated reciprocal asymmetry of TCF POP-1 and its coactivator beta-catenin SYS-1. Development 134 (2007) 2685-2695
23. Ishitani T., Ninomiya-Tsuji J., Nagai S., Nishita M., Meneghini M., Barker N., Waterman M., Bowerman B., Clevers H., Shibuya H., and Matsumoto K. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399 (1999) 798-802
24. Jantsch-Plunger V., Gonczy P., Romano A., Schnabel H., Hamill D., Schnabel R., Hyman A.A., and Glotzer M. CYK-4: a Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149 (2000) 1391-1404
25. Kaletta T., Schnabel H., and Schnabel R. Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390 (1997) 294-298
26. Kidd III A.R., Miskowski J.A., Siegfried K.R., Sawa H., and Kimble J. A beta-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 121 (2005) 761-772
27. Kohn A.D., and Moon R.T. Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38 (2005) 439-446
28. Köppen M., Simske J.S., Sims P.A., Firestein B.L., Hall D.H., Radice A.D., Rongo C., and Hardin J.D. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3 (2001) 983-991
29. Korswagen H.C. Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans: variations on a common signaling theme. Bioessays 24 (2002) 801-810
30. Kuhl M. Non-canonical Wnt signaling in Xenopus: regulation of axis formation and gastrulation. Semin. Cell Dev. Biol. 13 (2002) 243-249
31. Kuhl M., Geis K., Sheldahl L.C., Pukrop T., Moon R.T., and Wedlich D. Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. Mech. Dev. 106 (2001) 61-76
32. Lee J.Y., Marston D.J., Walston T., Hardin J., Halberstadt A., and Goldstein B. Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr. Biol. 16 (2006) 1986-1997
33. Lo M.C., Gay F., Odom R., Shi Y., and Lin R. Phosphorylation by the beta-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans. Cell 117 (2004) 95-106
34. Meneghini M.D., Ishitani T., Carter J.C., Hisamoto N., Ninomiya-Tsuji J., Thorpe C.J., Hamill D.R., Matsumoto K., and Bowerman B. MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature 399 (1999) 793-797
35. Mizumoto K., and Sawa H. Cortical beta-catenin and APC regulate asymmetric nuclear beta-catenin localization during asymmetric cell division in C. elegans. Dev. Cell 12 (2007) 287-299
36. Mizumoto K., and Sawa H. Two betas or not two betas: regulation of asymmetric division by beta-catenin. Trends Cell Biol. 17 (2007) 465-473
37. Mlodzik M. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation?. Trends Genet. 18 (2002) 564-571
38. Mohler W.A., Shemer G., del Campo J.J., Valansi C., Opoku-Serebuoh E., Scranton V., Assaf N., White J.G., and Podbilewicz B. The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev. Cell 2 (2002) 355-362
39. Moon R.T., Brown J.D., and Torres M. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet. 13 (1997) 157-162
40. Moriguchi T., Kawachi K., Kamakura S., Masuyama N., Yamanaka H., Matsumoto K., Kikuchi A., and Nishida E. Distinct domains of mouse dishevelled are responsible for the c-Jun N-terminal kinase/stress-activated protein kinase activation and the axis formation in vertebrates. J. Biol. Chem. 274 (1999) 30,957-30,962
41. Nakamura K., Kim S., Ishidate T., Bei Y., Pang K., Shirayama M., Trzepacz C., Brownell D.R., and Mello C.C. Wnt signaling drives WRM-1/beta-catenin asymmetries in early C. elegans embryos. Genes Dev. 19 (2005) 1749-1754
42. Noselli S., and Agnes F. Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr. Opin. Genet. Dev. 9 (1999) 466-472
43. Paricio N., Feiguin F., Boutros M., Eaton S., and Mlodzik M. The Drosophila STE20-like kinase misshapen is required downstream of the Frizzled receptor in planar polarity signaling. EMBO J. 18 (1999) 4669-4678
44. Park F.D., and Priess J.R. Establishment of POP-1 asymmetry in early C. elegans embryos. Development 130 (2003) 3547-3556
45. Penton A., Wodarz A., and Nusse R. A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin. Genetics 161 (2002) 747-762
46. Phillips B.T., Kidd III A.R., King R., Hardin J., and Kimble J. Reciprocal asymmetry of SYS-1/beta-catenin and POP-1/TCF controls asymmetric divisions in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 3231-3236
47. Piekny A.J., and Mains P.E. Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J. Cell. Sci. 115 (2002) 2271-2282
48. Piekny A.J., Wissmann A., and Mains P.E. Embryonic morphogenesis in Caenorhabditis elegans integrates the activity of LET-502 Rho-binding kinase, MEL-11 myosin phosphatase, DAF-2 insulin receptor and FEM-2 PP2c phosphatase. Genetics 156 (2000) 1671-1689
49. Poinat P., De Arcangelis A., Sookhareea S., Zhu X., Hedgecock E.M., Labouesse M., and Georges-Labouesse E. A conserved interaction between beta1 integrin/PAT-3 and Nck-interacting kinase/MIG-15 that mediates commissural axon navigation in C. elegans. Curr. Biol. 12 (2002) 622-631
50. Raich W.B., Agbunag C., and Hardin J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr. Biol. 9 (1999) 1139-1146
51. Raich W.B., Moran A.N., Rothman J.H., and Hardin J. Cytokinesis and midzone microtubule organization in Caenorhabditis elegans require the kinesin-like protein ZEN-4. Mol. Biol. Cell 9 (1998) 2037-2049
52. Rocheleau C.E., Yasuda J., Shin T.H., Lin R., Sawa H., Okano H., Priess J.R., Davis R.J., and Mello C.C. WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 97 (1999) 717-726
53. Rothbacher U., Laurent M.N., Deardorff M.A., Klein P.S., Cho K.W., and Fraser S.E. Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. EMBO J. 19 (2000) 1010-1022
54. Schlesinger A., Shelton C.A., Maloof J.N., Meneghini M., and Bowerman B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 13 (1999) 2028-2038
55. Schnabel R., Bischoff M., Hintze A., Schulz A.K., Hejnol A., Meinhardt H., and Hutter H. Global cell sorting in the C. elegans embryo defines a new mechanism for pattern formation. Dev. Biol. 294 (2006) 418-431
56. Sheldahl L.C., Slusarski D.C., Pandur P., Miller J.R., Kuhl M., and Moon R.T. Dishevelled activates Ca2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161 (2003) 769-777
57. Shin T.H., Yasuda J., Rocheleau C.E., Lin R., Soto M., Bei Y., Davis R.J., and Mello C.C. MOM-4, a MAP kinase kinase kinase-related protein, activates WRM-1/LIT-1 kinase to transduce anterior/posterior polarity signals in C. elegans. Mol. Cell 4 (1999) 275-280
58. Siegfried K.R., Kidd III A.R., Chesney M.A., and Kimble J. The sys-1 and sys-3 genes cooperate with Wnt signaling to establish the proximal-distal axis of the Caenorhabditis elegans gonad. Genetics 166 (2004) 171-186
59. Smit L., Baas A., Kuipers J., Korswagen H., van de Wetering M., and Clevers H. Wnt activates the Tak1/Nemo-like kinase pathway. J. Biol. Chem. 279 (2004) 17,232-17,240
60. Sokol S. A role for Wnts in morpho-genesis and tissue polarity. Nat. Cell Biol. 2 (2000) E124-E125
61. Spencer A.G., Orita S., Malone C.J., and Han M. A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13,132-13,137
62. Su Y.C., Maurel-Zaffran C., Treisman J.E., and Skolnik E.Y. The Ste20 kinase misshapen regulates both photoreceptor axon targeting and dorsal closure, acting downstream of distinct signals. Mol. Cell. Biol. 20 (2000) 4736-4744
63. Thomas-Virnig C.L., Sims P.A., Simske J.S., and Hardin J. The inositol 1,4,5-trisphosphate receptor regulates epidermal cell migration in Caenorhabditis elegans. Curr. Biol. 14 (2004) 1882-1887
64. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., and Moon R.T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13 (2003) 680-685
65. Wallingford J.B., and Habas R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132 (2005) 4421-4436
66. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., and Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405 (2000) 81-85
67. Walston T., Guo C., Proenca R., Wu M., Herman M., Hardin J., and Hedgecock E. mig-5/Dsh Controls Cell Fate Determination and Cell Migration in C. elegans. in prep (2006)
68. Walston T., Tuskey C., Edgar L., Hawkins N., Ellis G., Bowerman B., Wood W., and Hardin J. Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev. Cell 7 (2004) 831-841
69. Wang J., and Wilkinson M.F. Deletion mutagenesis of large (12-kb) plasmids by a one-step PCR protocol. Biotechniques 31 (2001) 722-724
70. Weaver C., and Kimelman D. Move it or lose it: axis specification in Xenopus. Development 131 (2004) 3491-3499
71. Wharton Jr. K.A. Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev. Biol. 253 (2003) 1-17
72. Williams-Masson E.M., Heid P.J., Lavin C.A., and Hardin J. The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis. Dev. Biol. 204 (1998) 263-276
73. Williams-Masson E.M., Malik A.N., and Hardin J. An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124 (1997) 2889-2901
74. Wissmann A., Ingles J., McGhee J.D., and Mains P.E. Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev. 11 (1997) 409-422
75. Wu M., and Herman M.A. Asymmetric localizations of LIN-17/Fz and MIG-5/Dsh are involved in the asymmetric B cell division in C. elegans. Dev. Biol. 303 (2007) 650-662
76. Yamaguchi T.P. Heads or tails: Wnts and anterior-posterior patterning. Curr. Biol. 11 (2001) R713-R724
77. Zar J.H. "Biostatistical Analysis" (1999), Prentice Hall, Upper Saddle River, NJ