Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling

Genes and Development

Volumn 22, Issue 21, 2008, Pages 3050-3063

  Li, Yan ^a,c   Rankin, Scott A ^a   Sinner, Débora ^a   Kenny, Alan P ^a   Krieg, Paul A ^b   Zorn, Aaron M ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c KUNMING INSTITUTE OF BOTANY   (China)

Author keywords

Foregut; Liver; Morphogenesis; Pancreas; Sfrp5; Wnt11

Indexed keywords

BETA CATENIN; MEMBRANE PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 5; UNCLASSIFIED DRUG; WNT11 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL FATE; CELL MOTION; CONTROLLED STUDY; GENE EXPRESSION; MORPHOGENESIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECRETION;

ANIMALS; CELL MOVEMENT; ENDODERM; EPITHELIUM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MORPHOGENESIS; SIGNAL TRANSDUCTION; WNT PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 55749083733     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1687308     Document Type: Article

References (73)

1. Axelrod, J.D., Miller, J.R., Shulman, J.M., Moon, R.T., and Perrimon, N. 1998. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes & Dev. 12: 2610-2622.
2. Bilic, J., Huang, Y.L., Davidson, G., Zimmermann, T., Cruciat, C.M., Bienz, M., and Niehrs, C. 2007. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316: 1619-1622.
3. Bort, R., Signore, M., Tremblay, K., Barbera, J.P., and Zaret, K.S. 2006. Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev. Biol. 290: 44-56.
4. Boutros, M., Paricio, N., Strutt, D.I., and Mlodzik, M. 1998. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94: 109-118.
5. Caneparo, L., Huang, Y.L., Staudt, N., Tada, M., Ahrendt, R., Kazanskaya, O., Niehrs, C., and Houart, C. 2007. Dickkopf-1 regulates gastrulation movements by coordinated modulation of Wnt/β catenin and Wnt/PCP activities, through interaction with the Dally-like homolog Knypek. Genes & Dev. 21: 465-480.
6. Chalmers, A.D. and Slack, J.M. 2000. The Xenopus tadpole gut: Fate maps and morphogenetic movements. Development 127: 381-392.
7. Cheyette, B.N., Waxman, J.S., Miller, J.R., Takemaru, K., Sheldahl, L.C., Khlebtsova, N., Fox, E.P., Earnest, T., and Moon, R.T. 2002. Dapper, a Dishevelled-associated antagonist of β-catenin and JNK signaling, is required for notochord formation. Dev. Cell 2: 449-461.
8. Clevers, H. 2006. Wnt/β-catenin signaling in development and disease. Cell 127: 469-480.
9. Dollar, G.L., Weber, U., Mlodzik, M., and Sokol, S.Y. 2005. Regulation of Lethal giant larvae by Dishevelled. Nature 437: 1376-1380.
10. Domingos, P.M., Itasaki, N., Jones, C.M., Mercurio, S., Sargent, M.G., Smith, J.C., and Krumlauf, R. 2001. The Wnt/β-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signalling. Dev. Biol. 239: 148-160.
11. Finley, K.R., Tennessen, J., and Shawlot, W. 2003. The mouse secreted frizzled-related protein 5 gene is expressed in the anterior visceral endoderm and foregut endoderm during early post-implantation development. Gene Expr. Patterns 3: 681-684.
12. Foley, A.C. and Mercola, M. 2005. Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex. Genes & Dev. 19: 387-396.
13. Galli, L.M., Barnes, T., Cheng, T., Acosta, L., Anglade, A., Willert, K., Nusse, R., and Burrus, L.W. 2006. Differential inhibition of Wnt-3a by Sfrp-1, Sfrp-2, and Sfrp-3. Dev. Dyn. 235: 681-690.
14. Garriock, R.J., D'Agostino, S.L., Pilcher, K.C., and Krieg, P.A. 2005. Wnt11-R, a protein closely related to mammalian Wnt11, is required for heart morphogenesis in Xenopus. Dev. Biol. 279: 179-192.
15. Gerhart, J. and Keller, R. 1986. Region-specific cell activities in amphibian gastrulation. Annu. Rev. Cell Biol. 2: 201-229.
16. Glinka, A., Wu, W., Delius, H., Monaghan, A.P., Blumenstock, C., and Niehrs, C. 1998. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391: 357-362.
17. Grapin-Botton, A. 2005. Antero-posterior patterning of the vertebrate digestive tract: 40 years after Nicole Le Douarin's Ph.D. thesis. Int. J. Dev. Biol. 49: 335-347.
18. Habas, R., Dawid, I.B., and He, X. 2003. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes & Dev. 17: 295-309.
19. 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. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
20. Horb, M.E. and Slack, J.M. 2001. Endoderm specification and differentiation in Xenopus embryos. Dev. Biol. 236: 330-343.
21. Kawano, Y. and Kypta, R. 2003. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116: 2627-2634.
22. Keller, R.E. 1975. Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer. Dev. Biol. 42: 222-241.
23. Kemp, C., Willems, E., Abdo, S., Lambiv, L., and Leyns, L. 2005. Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev. Dyn. 233: 1064-1075.
24. Kim, G.H. and Han, J.K. 2005. JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev. Dyn. 232: 958-968.
25. Kinoshita, N., Iioka, H., Miyakoshi, A., and Ueno, N. 2003. PKCδ is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes & Dev. 17: 1663-1676.
26. 2+ signaling. Mech. Dev. 106: 61-76.
27. Larkin, K. and Danilchik, M.V. 1999. Ventral cell rearrangements contribute to anterior-posterior axis lengthening between neurula and tailbud stages in Xenopus laevis. Dev. Biol. 216: 550-560.
28. Leaf, I., Tennessen, J., Mukhopadhyay, M., Westphal, H., and Shawlot, W. 2006. Sfrp5 is not essential for axis formation in the mouse. Genesis 44: 573-578.
29. Leimeister, C., Bach, A., and Gessler, M. 1998. Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech. Dev. 75: 29-42.
30. Leyns, L., Bouwmeester, T., Kim, S.H., Piccolo, S., and De Robertis, E.M. 1997. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88: 747-756.
31. Liao, G., Tao, Q., Kofron, M., Chen, J.S., Schloemer, A., Davis, R.J., Hsieh, J.C., Wylie, C., Heasman, J., and Kuan, C.Y. 2006. Jun NH2-terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. 103: 16313-16318.
32. Macdonald, B.T., Semenov, M.V., and He, X. 2007. SnapShot: Wnt/β-catenin signaling. Cell 131: 1204.
33. Mao, B., Wu, W., Li, Y., Hoppe, D., Stannek, P., Glinka, A., and Niehrs, C. 2001. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411: 321-325.
34. Matsui, T., Raya, A., Kawakami, Y., Callol-Massot, C., Capdevila, J., Rodriguez-Esteban, C., and Izpisua Belmonte, J.C. 2005. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes & Dev. 19: 164-175.
35. McLin, V.A., Rankin, S.A., and Zorn, A.M. 2007. Repression of Wnt/β-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134: 2207-2217.
36. Mikels, A.J. and Nusse, R. 2006. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol. 4: e115. doi: 10.1371/journal.pbio.0040115.
37. Moore-Scott, B.A., Opoka, R., Lin, S.C., Kordich, J.J., and Wells, J.M. 2007. Identification of molecular markers that are expressed in discrete anterior-posterior domains of the endoderm from the gastrula stage to mid-gestation. Dev. Dyn. 236: 1997-2003.
38. Mukhopadhyay, M., Shtrom, S., Rodriguez-Esteban, C., Chen, L., Tsukui, T., Gomer, L., Dorward, D.W., Glinka, A., Grinberg, A., Huang, S.P., et al. 2001. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1: 423-434.
39. Nojima, M., Suzuki, H., Toyota, M., Watanabe, Y., Maruyama, R., Sasaki, S., Sasaki, Y., Mita, H., Nishikawa, N., Yamaguchi, K., et al. 2007. Frequent epigenetic inactivation of SFRP genes and constitutive activation of Wnt signaling in gastric cancer. Oncogene 26: 4699-4713.
40. Nomoto, S., Kinoshita, T., Kato, K., Otani, S., Kasuya, H., Takeda, S., Kanazumi, N., Sugimoto, H., and Nakao, A. 2007. Hypermethylation of multiple genes as clonal markers in multicentric hepatocellular carcinoma. Br. J. Cancer 97: 1260-1265.
41. Ogata, S., Morokuma, J., Hayata, T., Kolle, G., Niehrs, C., Ueno, N., and Cho, K.W. 2007. TGF-β signaling-mediated morphogenesis: Modulation of cell adhesion via cadherin endocytosis. Genes & Dev. 21: 1817-1831.
42. Oishi, I., Suzuki, H., Onishi, N., Takada, R., Kani, S., Ohkawara, B., Koshida, I., Suzuki, K., Yamada, G., Schwabe, G.C., et al. 2003. The receptor tyrosine kinase Ror2 is involved in noncanonical Wnt5a/JNK signalling pathway. Genes Cells 8: 645-654.
43. Pandur, P., Lasche, M., Eisenberg, L.M., and Kuhl, M. 2002. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418: 636-641.
44. Park, M. and Moon, R.T. 2002. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol. 4: 20-25.
45. Park, T.J., Gray, R.S., Sato, A., Habas, R., and Wallingford, J.B. 2005. Subcellular localization and signaling properties of dishevelled in developing vertebrate embryos. Curr. Biol. 15: 1039-1044.
46. Pilcher, K.E. and Krieg, P.A. 2002. Expression of the Wnt inhibitor, sFRP5, in the gut endoderm of Xenopus. Gene Expr. Patterns 2: 369-372.
47. Rothbächer, U., Laurent, M.N., Deardorff, M.A., Klein, P.S., Cho, K.W., and Fraser, S.E. 2000. Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. EMBO J. 19: 1010-1022.
48. Satoh, W., Gotoh, T., Tsunematsu, Y., Aizawa, S., and Shimono, A. 2006. Sfrp1 and Sfrp2 regulate anteroposterior axis elongation and somite segmentation during mouse embryogenesis. Development 133: 989-999.
49. Satoh, W., Matsuyama, M., Takemura, H., Aizawa, S., and Shimono, A. 2008. Sfrp1, Sfrp2, and Sfrp5 regulate the Wnt/β-catenin and the planar cell polarity pathways during early trunk formation in mouse. Genesis 46: 92-103.
50. Schambony, A. and Wedlich, D. 2007. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell 12: 779-792.
51. Semenov, M.V., Tamai, K., Brott, B.K., Kuhl, M., Sokol, S., and He, X. 2001. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11: 951-961.
52. Semenov, M.V., Habas, R., Macdonald, B.T., and He, X. 2007. SnapShot: Noncanonical Wnt signaling pathways. Cell 131: 1378.
53. 2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161: 769-777.
54. Shook, D.R., Majer, C., and Keller, R. 2004. Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev. Biol. 270: 163-185.
55. Sinner, D., Rankin, S., Lee, M., and Zorn, A.M. 2004. Sox17 and β-catenin cooperate to regulate the transcription of endodermal genes. Development 131: 3069-3080.
56. Sokol, S.Y., Klingensmith, J., Perrimon, N., and Itoh, K. 1995. Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. Development 121: 1637-1647.
57. Tada, M. and Smith, J.C. 2000. Xwnt11 is a target of Xenopus Brachyury: Regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127: 2227-2238.
58. Tahinci, E. and Symes, K. 2003. Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. Dev. Biol. 259: 318-335.
59. Tao, Q., Yokota, C., Puck, H., Kofron, M., Birsoy, B., Yan, D., Asashima, M., Wylie, C.C., Lin, X., and Heasman, J. 2005. Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120: 857-871.
60. Topol, L., Jiang, X., Choi, H., Garrett-Beal, L., Carolan, P.J., and Yang, Y. 2003. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J. Cell Biol. 162: 899-908.
61. Tzahor, E. and Lassar, A.B. 2001. Wnt signals from the neural tube block ectopic cardiogenesis. Genes & Dev. 15: 255-260.
62. Ulrich, F., Krieg, M., Schotz, E.M., Link, V., Castanon, I., Schnabel, V., Taubenberger, A., Mueller, D., Puech, P.H., and Heisenberg, C.P. 2005. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9: 555-564.
63. Wallingford, J.B. and Habas, R. 2005. The developmental biology of Dishevelled: An enigmatic protein governing cell fate and cell polarity. Development 132: 4421-4436.
64. Wallingford, J.B., Rowning, B.A., Vogeli, K.M., Rothbacher, U., Fraser, S.E., and Harland, R.M. 2000. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405: 81-85.
65. Wang, S., Krinks, M., and Moos Jr., M. 1997. Frzb-1, an antagonist of Wnt-1 and Wnt-8, does not block signaling by Wnts-3A, -5A, or -11. Biochem. Biophys. Res. Commun. 236: 502-504.
66. Wang, J., Hamblet, N.S., Mark, S., Dickinson, M.E., Brinkman, B.C., Segil, N., Fraser, S.E., Chen, P., Wallingford, J.B., and Wynshaw-Boris, A. 2006. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133: 1767-1778.
67. Wawrzak, D., Metioui, M., Willems, E., Hendrickx, M., de Genst, E., and Leyns, L. 2007. Wnt3a binds to several sFRPs in the nanomolar range. Biochem. Biophys. Res. Commun. 357: 1119-1123.
68. Winklbauer, R., Medina, A., Swain, R.K., and Steinbeisser, H. 2001. Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413: 856-860.
69. Witzel, S., Zimyanin, V., Carreira-Barbosa, F., Tada, M., and Heisenberg, C.P. 2006. Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. J. Cell Biol. 175: 791-802.
70. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S., and Nishida, E. 2002. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3: 69-75.
71. Zaret, K.S. 2002. Regulatory phases of early liver development: Paradigms of organogenesis. Nat. Rev. Genet. 3: 499-512.
72. Zeng, X., Huang, H., Tamai, K., Zhang, X., Harada, Y., Yokota, C., Almeida, K., Wang, J., Doble, B., Woodgett, J., et al. 2008. Initiation of Wnt signaling: Control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135: 367-375.
73. Zou, H., Molina, J.R., Harrington, J.J., Osborn, N.K., Klatt, K.K., Romero, Y., Burgart, L.J., and Ahlquist, D.A. 2005. Aberrant methylation of secreted frizzled-related protein genes in esophageal adenocarcinoma and Barrett's esophagus. Int. J. Cancer 116: 584-591.