A context-dependent combination of Wnt receptors controls axis elongation and leg development in a short germ insect

Development

Volumn 138, Issue 13, 2011, Pages 2793-2805

  Beermann, Anke ^a,b   Prühs, Romy ^a   Lutz, Rebekka ^a,b   Schröder, Reinhard ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b Institute für Zellbiologie   (Germany)

Author keywords

Axis elongation; Frizzled receptors; Short germ embryogenesis; Tribolium; Wnt signalling

Indexed keywords

ARROW RECEPTOR; FIBROBLAST GROWTH FACTOR; FRIZZLED 1 PROTEIN; FRIZZLED 2 PROTEIN; FRIZZLED 4 PROTEIN; FRIZZLED PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GROWTH; LEG LENGTHENING; MESODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRIBOLIUM;

ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FRIZZLED RECEPTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; LARVA; LOWER EXTREMITY; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RNA INTERFERENCE; TRIBOLIUM; WNT PROTEINS;

ARTHROPODA; COLEOPTERA; HEXAPODA; TRIBOLIUM (BEETLE); TRIBOLIUM CASTANEUM; VERTEBRATA;

EID: 79958153178     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.063644     Document Type: Article

References (66)

1. Angers, S., Salahpour, A. and Bouvier, M. (2002). Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu. Rev. Pharmacol. Toxicol. 42, 409-435.
2. Arnold, S. J., Stappert, J., Bauer, A., Kispert, A., Herrmann, B. G. and Kemler, R. (2000). Brachyury is a target gene of the Wnt/beta-catenin signaling pathway. Mech. Dev. 91, 249-258.
3. Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M. B., Deng, C., Taketo, M., Lewandoski, M. and Pourquié, O. (2008). A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat. Cell Biol. 10, 186-193.
4. Beermann, A. and Schröder, R. (2008). Sites of Fgf signalling and perception during embryogenesis of the beetle Tribolium castaneum. Dev. Genes Evol. 218, 153-167.
5. Beermann, A., Aranda, M. and Schröder, R. (2004). The Sp8 zinc-finger transcription factor is involved in allometric growth of the limbs in the beetle Tribolium castaneum. Development 131, 733-742.
6. Bénazéraf, B., Francois, P., Baker, R. E., Denans, N., Little, C. D. and Pourquié, O. (2010). A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature 466, 248-252.
7. Berns, N., Kusch, T., Schröder, R. and Reuter, R. (2008). Expression, function and regulation of Brachyenteron in the short germ insect Tribolium castaneum. Dev. Genes Evol. 218, 169-179.
8. Bhanot, P., Brink, M., Samos, C. H., Hsieh, J. C., Wang, Y., Macke, J. P., Andrew, D., Nathans, J. and Nusse, R. (1996). A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382, 225-230.
9. Bolognesi, R., Beermann, A., Farzana, L., Wittkopp, N., Lutz, R., Balavoine, G., Brown, S. J. and Schröder, R. (2008a). Tribolium Wnts: evidence for a larger repertoire in insects with overlapping expression patterns that suggest multiple redundant functions in embryogenesis. Dev. Genes Evol. 218, 193-202.
10. Bolognesi, R., Farzana, L., Fischer, T. D. and Brown, S. J. (2008b). Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr. Biol. 18, 1624-1629.
11. Bolognesi, R., Fischer, T. D. and Brown, S. J. (2009). Loss of Tc-arrow and canonical Wnt signaling alters posterior morphology and pair-rule gene expression in the short-germ insect, Tribolium castaneum. Dev. Genes Evol. 219, 369-375.
12. Brown, S. J., Parrish, J. K., Beeman, R. W. and Denell, R. E. (1997). Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum. Mech. Dev. 61, 165-173.
13. Bucher, G., Scholten, J. and Klingler, M. (2002). Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85-R86.
14. Cadigan, K. M. and Nusse, R. (1997). Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286-3305.
15. Carron, C., Pascal, A., Djiane, A., Boucaut, J.-C., Shi, D.-L. and Umbhauer, M. (2003). Frizzled receptor dimerization is sufficient to activate the Wnt/betacatenin pathway. J. Cell Sci. 116, 2541-2550.
16. Chen, C. M. and Struhl, G. (1999). Wingless transduction by the Frizzled and Frizzled2 proteins of Drosophila. Development 126, 5441-5452.
17. Choe, C. P., Miller, S. C. and Brown, S. J. (2006). A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc. Natl. Acad. Sci. USA 103, 6560-6564.
18. Cohen, B., Simcox, A. A. and Cohen, S. M. (1993). Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117, 597-608.
19. Cohen, S. M. and Jürgens, G. (1989). Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J. 8, 2045-2055.
20. Copf, T., Schröder, R. and Averof, M. (2004). Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl. Acad. Sci. USA 101, 17711-17715.
21. Dann, C. E., Hsieh, J. C., Rattner, A., Sharma, D., Nathans, J. and Leahy, D. J. (2001). Insights into Wnt binding and signalling from the structures of two Frizzled cysteine-rich domains. Nature 412, 86-90.
22. Delfini, M. C., Dubrulle, J., Malapert, P., Chal, J. and Pourquié, O. (2005). Control of the segmentation process by graded MAPK/ERK activation in the chick embryo. Proc. Natl. Acad. Sci. USA 102, 11343-11348.
23. Dequéant, M.-L. and Pourquié, O. (2008). Segmental patterning of the vertebrate embryonic axis. Nat. Rev. Genet. 9, 370-382.
24. Diaz-Benjumea, F. J. and Cohen, S. M. (1993). Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741-752.
25. Diaz-Benjumea, F. J. and Cohen, S. M. (1994). wingless acts through the shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg. Development 120, 1661-1670.
26. Grossmann, D., Scholten, J. and Prpic, N. M. (2009). Separable functions of wingless in distal and ventral patterning of the Tribolium leg. Dev. Genes Evol. 219, 469-479.
27. Habas, R. and Dawid, I. B. (2005). Dishevelled and Wnt signaling: is the nucleus the final frontier? J. Biol. 4, 2.
28. Hsieh, J. C., Rattner, A., Smallwood, P. M. and Nathans, J. (1999). Biochemical characterization of Wnt-frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc. Natl. Acad. Sci. USA 96, 3546-3551.
29. Huét, C. and Lenoir-Rousseaux, J. J. (1976). Étude de la mise en place de la patte imaginale de Tenebrio molitor. J. Embryol. Exp. Morphol. 35, 303-321.
30. Huson, D. H., Richter, D. C., Rausch, C., Dezulian, T., Franz, M. and Rupp, R. (2007). Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460.
31. Janssen, R., Le Gouar, M., Pechmann, M., Poulin, F., Bolognesi, R., Schwager, E. E., Hopfen, C., Colbourne, J. K., Budd, G. E., Brown, S. J. et al. (2010). Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol. Biol. 10, 374.
32. Kennerdell, J. R. and Carthew, R. W. (1998). Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95, 1017-1026.
33. Kim, H. S., Murphy, T., Xia, J., Caragea, D., Park, Y., Beeman, R. W., Lorenzen, M. D., Butcher, S., Manak, J. R. and Brown, S. J. (2010). BeetleBase in 2010, revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res. 38, D437-D442.
34. Klingseisen, A., Clark, I. B., Gryzik, T. and Muller, H. A. (2009). Differential and overlapping functions of two closely related Drosophila FGF8-like growth factors in mesoderm development. Development 136, 2393-2402.
35. Kubota, K., Goto, S. and Hayashi, S. (2003). The role of Wg signaling in the patterning of embryonic leg primordium in Drosophila. Dev. Biol. 257, 117-126.
36. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
37. Martin, B. L. and Kimelman, D. (2009). Wnt signaling and the evolution of embryonic posterior development. Curr. Biol. 19, R215-R219.
38. McGregor, A. P., Pechmann, M., Schwager, E. E., Feitosa, N. M., Kruck, S., Aranda, M. and Damen, W. G. (2008). Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr. Biol. 18, 1619-1623.
39. McMahon, A., Reeves, G. T., Supatto, W. and Stathopoulos, A. (2010). Mesoderm migration in Drosophila is a multi-step process requiring FGF signaling and integrin activity. Development 137, 2167-2175.
40. Milligan, G. (2004). G protein-coupled receptor dimerization: function and ligand pharmacology. Mol. Pharmacol. 66, 1-7.
41. Miyawaki, K., Mito, T., Sarashina, I., Zhang, H., Shinmyo, Y., Ohuchi, H. and Noji, S. (2004). Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech. Dev. 121, 119-130.
42. Ober, K. A. and Jockusch, E. L. (2006). The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev. Biol. 294, 391-405.
43. Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358.
44. Patel, N. (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol. 44, 445-487.
45. Patel, N. H., Condron, B. G. and Zinn, K. (1994). Pair-rule expression patterns of even-skipped are found in both short-and long-germ beetles. Nature 367, 429-434.
46. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
47. Pueyo, J. I., Galindo, M. I., Bishop, S. A. and Couso, J. P. (2000). Proximal-distal leg development in Drosophila requires the apterous gene and the Lim1 homologue dlim1. Development 127, 5391-5402.
48. Rulifson, E. J., Wu, C. H. and Nusse, R. (2000). Pathway specificity by the bifunctional receptor frizzled is determined by affinity for wingless. Mol. Cell 6, 117-126.
49. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning-A Laboratory Manual. Cold Spring Harbour Laboratory Press: Cold Spring Harbour, NY.
50. Schoppmeier, M. and Schröder, R. (2005). Maternal torso signaling controls body axis elongation in a short germ insect. Curr. Biol. 15, 2131-2136.
51. Schröder, R., Beermann, A., Wittkopp, N. and Lutz, R. (2008). From development to biodiversity-Tribolium castaneum, an insect model organism for short germband development. Dev. Genes Evol. 218, 119-126.
52. Schulte, G. and Bryja, V. (2007). The Frizzled family of unconventional G-proteincoupled receptors. Trends Pharmacol. Sci. 28, 518-525.
53. Stiegler, A. L., Burden, S. J. and Hubbard, S. R. (2009). Crystal structure of the frizzled-like cysteine-rich domain of the receptor tyrosine kinase MuSK. J. Mol. Biol. 393, 1-9.
54. Strimmer, K. and von Haeseler, A. (1996). Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964-969.
55. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530-535.
56. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
57. Tsuji, T., Sato, A., Hiratani, I., Taira, M., Saigo, K. and Kojima, T. (2000). Requirements of Lim1, a Drosophila LIM-homeobox gene, for normal leg and antennal development. Development 127, 4315-4323.
58. Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Riou, J. F., Boucaut, J. C. and Shi, D. L. (2000). The C-terminal cytoplasmic Lys-thr-X-X-XTrp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J. 19, 4944-4954.
59. van Amerongen, R. and Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214.
60. Van der Meer, J. M. (1977). Optical clean and permanent whole mount preparation for phase-contrast microscopy of cuticular sructures of insect larvae. Drosophila Inf. Serv. 52, 160.
61. Wehrli, M., Dougan, S. T., Caldwell, K., O'Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A. and DiNardo, S. (2000). arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407, 527-530.
62. Widelitz, R. (2005). Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 23, 111-116.
63. Wu, J. and Mlodzik, M. (2008). The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev. Cell 15, 462-469.
64. Wu, J., Klein, T. J. and Mlodzik, M. (2004). Subcellular localization of frizzled receptors, mediated by their cytoplasmic tails, regulates signaling pathway specificity. PloS Biol. 2, E158.
65. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.
66. Yang-Snyder, J., Miller, J. R., Brown, J. D., Lai, C. J. and Moon, R. T. (1996). A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6, 1302-1306.