The β-catenin HMP-2 functions downstream of Src in parallel with the Wnt pathway in early embryogenesis of C. elegans

Developmental Biology

Volumn 355, Issue 2, 2011, Pages 302-312

  Sumiyoshi, Eisuke ^a,b   Takahashi, Sachiko ^a   Obata, Hatsue ^a   Sugimoto, Asako ^b,c   Kohara, Yuji ^a  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

C. elegans; Endoderm induction; Src signal; Wnt signal; catenin

Indexed keywords

BETA CATENIN; BETA CATENIN HMP 2; PROTEIN TYROSINE KINASE; STEROID RECEPTOR COACTIVATOR 1; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; BLASTOMERE; CAENORHABDITIS ELEGANS; CELL DIVISION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWNSTREAM PROCESSING; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPINDLE CELL;

CAENORHABDITIS ELEGANS;

EID: 79959247656     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.04.034     Document Type: Article

References (45)

1. Baugh L.R., Hill A.A., Slonim D.K., Brown E.L., Hunter C.P. Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 2003, 130:889-900.
2. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 1996, 382:638-642.
3. Bei Y., Hogan J., Berkowitz L.A., Soto M., Rocheleau C.E., Pang K.M., Collins J., Mello C.C. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev. Cell 2002, 3:113-125.
4. Berkowitz L.A., Strome S. MES-1, a protein required for unequal divisions of the germline in early C. elegans embryos, resembles receptor tyrosine kinases and is localized to the boundary between the germline and gut cells. Development 2000, 127:4419-4431.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Broitman-Maduro G., Lin K.T., Hung W.W., Maduro M.F. Specification of the C. elegans MS blastomere by the T-box factor TBX-35. Development 2006, 133:3097-3106.
7. Bryant D.M., Stow J.L. The ins and outs of E-cadherin trafficking. Trends Cell Biol. 2004, 14:427-434.
8. Calvo D., Victor M., Gay F., Sui G., Luke M.P., Dufourcq P., Wen G., Maduro M., Rothman J., Shi Y. A POP-1 repressor complex restricts inappropriate cell type-specific gene transcription during Caenorhabditis elegans embryogenesis. EMBO J. 2001, 20:7197-7208.
9. Costa M., Raich W., Agbunag C., Leung B., Hardin J., Priess J.R. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 1998, 141:297-308.
10. Daniel J.M. Dancing in and out of the nucleus: p120(ctn) and the transcription factor Kaiso. Biochim. Biophys. Acta 2007, 1773:59-68.
11. Daugherty R.L., Gottardi C.J. Phospho-regulation of Beta-catenin adhesion and signaling functions. Physiology (Bethesda) 2007, 22:303-309.
12. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
13. Goldstein B. An analysis of the response to gut induction in the C. elegans embryo. Development 1995, 121:1227-1236.
14. Grana T.M., Cox E.A., Lynch A.M., Hardin J. SAX-7/L1CAM and HMR-1/cadherin function redundantly in blastomere compaction and non-muscle myosin accumulation during Caenorhabditis elegans gastrulation. Dev. Biol. 2010, 344:731-744.
15. Hayashizaki S., Iino Y., Yamamoto M. Characterization of the C. elegans gap-2 gene encoding a novel Ras-GTPase activating protein and its possible role in larval development. Genes Cells 1998, 3:189-202.
16. Huang S., Shetty P., Robertson S.M., 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 2007, 134:2685-2695.
17. Huelsken J., Behrens J. The Wnt signalling pathway. J. Cell Sci. 2002, 115:3977-3978.
18. Kam Y., Quaranta V. Cadherin-bound beta-catenin feeds into the Wnt pathway upon adherens junctions dissociation: evidence for an intersection between beta-catenin pools. PLoS One 2009, 4:e4580.
19. Kidd A.R., Miskowski J.A., Siegfried K.R., Sawa H., Kimble J. A beta-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 2005, 121:761-772.
20. Kinoshita E., Kinoshita-Kikuta E., Takiyama K., Koike T. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 2006, 5:749-757.
21. Korswagen H.C., Herman M.A., Clevers H.C. Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature 2000, 406:527-532.
22. Laufer J.S., Bazzicalupo P., Wood W.B. Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 1980, 19:569-577.
23. Lilien J., Balsamo J. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin. Curr. Opin. Cell Biol. 2005, 17:459-465.
24. Lin R., Thompson S., Priess J.R. pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 1995, 83:599-609.
25. Lin R., Hill R.J., Pries J.R. POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 1998, 92:229-239.
26. Liu J., Phillips B.T., Amaya M.F., Kimble J., Xu W. The C. elegans SYS-1 protein is a bona fide beta-catenin. Dev. Cell 2008, 14:751-761.
27. Liu J., Maduzia L.L., Shirayama M., Mello C.C. NMY-2 maintains cellular asymmetry and cell boundaries, and promotes a SRC-dependent asymmetric cell division. Dev. Biol. 2010, 339:366-373.
28. Lo M.C., Gay F., Odom R., Shi Y., 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 2004, 117:95-106.
29. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
30. Maduro M.F., Lin R., Rothman J.H. Dynamics of a developmental switch: recursive intracellular and intranuclear redistribution of Caenorhabditis elegans POP-1 parallels Wnt-inhibited transcriptional repression. Dev. Biol. 2002, 248:128-142.
31. Maduro M.F., Hill R.J., Heid P.J., Newman-Smith E.D., Zhu J., Priess J.R., Rothman J.H. Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev. Biol. 2005, 284:509-522.
32. Maloof J.N., Whangbo J., Harris J.M., Jongeward G.D., Kenyon C. A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans. Development 1999, 126:37-49.
33. Miller D.M., Shakes D.C. Immunofluorescence microscopy. Methods Cell Biol. 1995, 48:365-394.
34. Natarajan L., Witwer N.E., Eisenmann D.M. The divergent Caenorhabditis elegans beta-catenin proteins BAR-1, WRM-1 and HMP-2 make distinct protein interactions but retain functional redundancy in vivo. Genetics 2001, 159:159-172.
35. Natarajan L., Jackson B.M., Szyleyko E., Eisenmann D.M. Identification of evolutionarily conserved promoter elements and amino acids required for function of the C. elegans beta-catenin homolog BAR-1. Dev. Biol. 2004, 272:536-557.
36. Nelson W.J., Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004, 303:1483-1487.
37. Pettitt J., Cox E.A., Broadbent I.D., Flett A., Hardin J. The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J. Cell Biol. 2003, 162:15-22.
38. Putzke A.P., Rothman J.H. Repression of Wnt signaling by a Fer-type nonreceptor tyrosine kinase. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16154-16159.
39. Rocheleau C.E., Downs W.D., Lin R., Wittmann C., Bei Y., Cha Y.H., Ali M., Priess J.R., Mello C.C. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 1997, 90:707-716.
40. Rocheleau C.E., Yasuda J., Shin T.H., Lin R., Sawa H., Okano H., Priess J.R., Davis R.J., Mello C.C. WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 1999, 97:717-726.
41. Sugioka K., Sawa H. Regulation of asymmetric positioning of nuclei by Wnt and Src signaling and its roles in POP-1/TCF nuclear asymmetry in Caenorhabditis elegans. Genes Cells 2010, 15:397-407.
42. Shetty P., Lo M.C., Robertson S.M., Lin R. C. elegans TCF protein, POP-1 converts from repressor to activator as a result of Wnt-induced lowering of nuclear levels. Dev. Biol. 2005, 285:584-592.
43. Thorpe C.J., Schlesinger A., Carter J.C., Bowerman B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 1997, 90:695-705.
44. Walston T., Tuskey C., Edgar L., Hawkins N., Ellis G., Bowerman B., Wood W., Hardin J. Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev. Cell 2004, 7:831-841.
45. Zaidel-Bar R., Joyce M.J., Lynch A.M., Witte K., Audhya A., Hardin J. The F-BAR domain of SRGP-1 facilitates cell-cell adhesion during C. elegans morphogenesis. J. Cell Biol. 2010, 191:761-769.