Intestinal tube formation in Caenorhabditis elegans requires vang-1 and egl-15 signaling

Developmental Biology

Volumn 339, Issue 2, 2010, Pages 268-279

  Hoffmann, Michael ^b   Segbert, Christoph ^b   Helbig, Gisela ^b   Bossinger, Olaf ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Caenorhabditis elegans; Cell intercalation; Epithelium; FGF signaling; Intercellular junctions; Intestine; Organogenesis; Planar cell polarity; Wnt signaling

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; PDZ 2 PROTEIN; PDZ PROTEIN; PROTEIN EGL 15; PROTEIN TYROSINE KINASE; PROTEIN VANG 1; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL POLARITY; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; EPITHELIUM CELL; GENE FUNCTION; GENE LOCATION; GENE OVEREXPRESSION; INTESTINE; INTESTINE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

CAENORHABDITIS ELEGANS;

EID: 76949106061     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.12.002     Document Type: Article

References (70)

1. Axelrod J., and McNeill H. Coupling planar cell polarity signaling to morphogenesis. ScientificWorldJournal 2 (2002) 434-454
2. Bastock R., Strutt H., and Strutt D. Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130 (2003) 3007-3014
3. Bellaiche Y., Beaudoin-Massiani O., Stuttem I., and Schweisguth F. The planar cell polarity protein Strabismus promotes Pins anterior localization during asymmetric division of sensory organ precursor cells in Drosophila. Development 131 (2004) 469-478
4. Bertet C., Sulak L., and Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429 (2004) 667-671
5. Blom N., Gammeltoft S., and Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294 (1999) 1351-1362
6. Bossinger O., Klebes A., Segbert C., Theres C., and Knust E. Zonula adherens formation in Caenorhabditis elegans requires dlg-1, the homologue of the Drosophila gene discs large. Dev. Biol. 230 (2001) 29-42
7. Bossinger O., Fukushige T., Claeys M., Borgonie G., and McGhee J.D. The apical disposition of the Caenorhabditis elegans intestinal terminal web is maintained by LET-413. Dev. Biol. 268 (2004) 448-456
8. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
9. Bülow H.E., Boulin T., and Hobert O. Differential functions of the C. elegans FGF receptor in axon outgrowth and maintenance of axon position. Neuron 42 (2004) 367-374
10. Carberry K., Wiesenfahrt T., Windoffer R., Bossinger O., and Leube R.E. Intermediate filaments in Caenorhabditis elegans. Cell Motil. Cytoskeleton 66 (2009) 852-864
11. 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
12. Chen L., Ong B., and Bennett V. LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J. Cell. Biol. 154 (2001) 841-855
13. Chen J.R., Chang B.H., Allen J.E., Stiffler M.A., and Macbeath G. Predicting PDZ domain-peptide interactions from primary sequences. Nat. Biotechnol. 26 (2008) 1041-1045
14. Ciruna B., Jenny A., Lee D., Mlodzik M., and Schier A.F. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439 (2006) 220-224
15. Darken R.S., Scola A.M., Rakeman A.S., Das G., Mlodzik M., and Wilson P.A. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J. 21 (2002) 976-985
16. Doudney K., and Stanier P. Epithelial cell polarity genes are required for neural tube closure. Am. J. Med. Genet. C Semin. Med. Genet. 135 (2005) 42-47
17. Fukushige T., Hawkins M.G., and McGhee J.D. The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev. Biol. 198 (1998) 286-302
18. Fukushige T., Hendzel M.J., Bazett-Jones D.P., and McGhee J.D. Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11883-11888
19. Gomes J.E., Corado M., and Schweisguth F. Van Gogh and Frizzled act redundantly in the Drosophila sensory organ precursor cell to orient its asymmetric division. PLoS ONE 4 (2009) e4485
20. Goto T., and Keller R. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev. Biol. 247 (2002) 165-181
21. Green J., Inoue T., and Sternberg P. Opposing Wnt pathways orient cell polarity during organogenesis. Cell 134 (2008) 646-656
22. Hawkins M., and McGhee J. elt-2, a second GATA factor from the nematode Caenorhabditis elegans. J. Biol. Chem. 270 (1995) 14666-14671
23. 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
24. Hermann G.J., Leung B., and Priess J.R. Left-right asymmetry in C. elegans intestine organogenesis involves a LIN-12/Notch signaling pathway. Development 127 (2000) 3429-3440
25. 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 beta-catenin independent Wnt pathway. Dev. Biol. 328 (2009) 245-256
26. Huang P., and Stern M.J. FGF signaling functions in the hypodermis to regulate fluid balance in C. elegans. Development 131 (2004) 2595-2604
27. Hüsken K., Wiesenfahrt T., Abraham C., Windoffer R., Bossinger O., and Leube R. Maintenance of the intestinal tube in Caenorhabditis elegans: the role of the intermediate filament protein IFC-2. Differentiation 76 (2008) 881-896
28. Kallay L.M., McNickle A., Brennwald P.J., Hubbard A.L., and Braiterman L.T. Scribble associates with two polarity proteins, Lgl2 and Vangl2, via distinct molecular domains. J. Cell. Biochem. 99 (2006) 647-664
29. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298 (2002) 1950-1954
30. Keller R., Shook D., and Skoglund P. The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys. Biol. 5 (2008) 15007
31. Kibar Z., Vogan K.J., Groulx N., Justice M.J., Underhill D.A., and Gros P. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet. 28 (2001) 251-255
32. King R.S., Maiden S.L., Hawkins N.C., Kidd III A.R., Kimble J., Hardin J., and Walston T.D. The N- or C-terminal domains of DSH-2 can activate the C. elegans Wnt/beta-catenin asymmetry pathway. Dev. Biol. 328 (2009) 234-244
33. Korswagen H. Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans: variations on a common signaling theme. Bioessays 24 (2002) 801-810
34. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
35. Kuchinke U., Grawe F., and Knust E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 8 (1998) 1357-1365
36. Labouesse M. Epithelial junctions and attachments. WormBook (2006)
37. Lake B.B., and Sokol S.Y. Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. J. Cell. Biol. 185 (2009) 59-66
38. Lee O.K., Frese K.K., James J.S., Chadda D., Chen Z.H., Javier R.T., and Cho K.O. Discs-large and strabismus are functionally linked to plasma membrane formation. Nat. Cell. Biol. 5 (2003) 987-993
39. Lee H.S., Mood K., Battu G., Ji Y.J., Singh A., and Daar I.O. Fibroblast growth factor receptor-induced phosphorylation of ephrinB1 modulates its interaction with Dishevelled. Mol. Biol. Cell. 20 (2009) 124-133
40. Legouis R., Gansmuller A., Sookhareea S., Bosher J.M., Baillie D.L., and Labouesse M. LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat. Cell. Biol. 2 (2000) 415-422
41. Legouis R., Jaulin-Bastard F., Schott S., Navarro C., Borg J.P., and Labouesse M. Basolateral targeting by leucine-rich repeat domains in epithelial cells. EMBO Rep. 4 (2003) 1096-1100
42. Leung B., Hermann G.J., and Priess J.R. Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216 (1999) 114-134
43. Lockwood C.A., Lynch A.M., and Hardin J. Dynamic analysis identifies novel roles for DLG-1 subdomains in AJM-1 recruitment and LET-413-dependent apical focusing. J. Cell. Sci. 121 (2008) 1477-1487
44. Lynch A.M., and Hardin J. The assembly and maintenance of epithelial junctions in C. elegans. Front. Biosci. 14 (2009) 1414-1432
45. Matsuyama M., Aizawa S., and Shimono A. Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet. 5 (2009) e1000427
46. McGhee J.D. The C. elegans intestine. WormBook (2007)
47. McMahon L., Legouis R., Vonesch J.L., and Labouesse M. Assembly of C. elegans apical junctions involves positioning and compaction by LET-413 and protein aggregation by the MAGUK protein DLG-1. J. Cell. Sci. 114 (2001) 2265-2277
48. Montcouquiol M., Rachel R., Lanford P., Copeland N., Jenkins N., and Kelley M. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423 (2003) 173-177
49. Park F.D., Tenlen J.R., and Priess J.R. C. elegans MOM-5/frizzled functions in MOM-2/Wnt-independent cell polarity and is localized asymmetrically prior to cell division. Curr. Biol. 14 (2004) 2252-2258
50. Podbilewicz B., and White J. Cell fusions in the developing epithelia of C. elegans. Dev. Biol. 161 (1994) 408-424
51. Segbert C., Johnson K., Theres C., van Fürden D., and Bossinger O. Molecular and functional analysis of apical junction formation in the gut epithelium of Caenorhabditis elegans. Dev. Biol. 266 (2004) 17-26
52. Shi W., Peyrot S.M., Munro E., and Levine M. FGF3 in the floor plate directs notochord convergent extension in the Ciona tadpole. Development 136 (2009) 23-28
53. Songyang Z., Fanning A., Fu C., Xu J., Marfatia S., Chishti A., Crompton A., Chan A., Anderson J., and Cantley L. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275 (1997) 73-77
54. Sonnhammer E., Eddy S., Birney E., Bateman A., and Durbin R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res. 26 (1998) 320-322
55. Strome S., and Wood W.B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35 (1983) 15-25
56. Strutt D. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7 (2001) 367-375
57. Strutt D. The planar polarity pathway. Curr. Biol. 18 (2008) R898-R902
58. Sulston J., Schierenberg E., White J., and Thomson J. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100 (1983) 64-119
59. Taylor J., Abramova N., Charlton J., and Adler P.N. Van Gogh: a new Drosophila tissue polarity gene. Genetics 150 (1998) 199-210
60. Tonikian R., Zhang Y., Sazinsky S.L., Currell B., Yeh J.H., Reva B., Held H.A., Appleton B.A., Evangelista M., Wu Y., Xin X., Chan A.C., Seshagiri S., Lasky L.A., Sander C., Boone C., Bader G.D., and Sidhu S.S. A specificity map for the PDZ domain family. PLoS Biol. e239 (2008) 6
61. Tree D., Ma D., and Axelrod J. A three-tiered mechanism for regulation of planar cell polarity. Semin. Cell Dev. Biol. 13 (2002) 217-224
62. Wallingford J.B., Fraser S.E., and Harland R.M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2 (2002) 695-706
63. Walston T., Guo C., Proenca R., Wu M., Herman M.A., Hardin J., and Hedgecock E.M. mig-5/Dsh controls cell fate determination and cell migration in C. elegans. Dev. Biol. 298 (2006) 485-497
64. Wang Y., and Nathans J. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134 (2007) 647-658
65. Wodarz A., and Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell. Dev. Biol. 14 (1998) 59-88
66. Wodarz A., Ramrath A., Kuchinke U., and Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402 (1999) 544-547
67. Wolff T., and Rubin G. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125 (1998) 1149-1159
68. Wu M., and Herman M.A. A novel noncanonical Wnt pathway is involved in the regulation of the asymmetric B cell division in C. elegans. Dev. Biol. 293 (2006) 316-329
69. 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
70. Wu J., and Mlodzik M. A quest for the mechanism regulating global planar cell polarity of tissues. Trends Cell. Biol. 19 (2009) 295-305