LRP6 exerts non-canonical effects on Wnt signaling during neural tube closure

Human Molecular Genetics

Volumn 22, Issue 21, 2013, Pages 4267-4281

  Gray, Jason D ^a,c   Kholmanskikh, Stanislav ^a   Castaldo, Bozena S ^a   Hansler, Alex ^b   Chung, Heekyung ^b,d   Klotz, Brian ^a   Singh, Shawn ^a   Brown, Anthony M C ^b   Ross, M Elizabeth ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN2; BETA CATENIN; DISHEVELED ASSOCIATED ACTIVATOR OF MORPHOGENESIS 1; F ACTIN; GAMMA TUBULIN; GUANOSINE TRIPHOSPHATASE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MESSENGER RNA; PROTEIN; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; WNT PROTEIN; WNT5A PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL POLARITY; CELL PROLIFERATION; CELL SHAPE; CENTROSOME; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; GASTRULATION; GENE EXPRESSION; MOUSE; NEURAL TUBE; NEURULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALLELES; ANIMALS; CELL POLARITY; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; NEURAL CREST; NEURAL TUBE; NEURULATION; NIH 3T3 CELLS; PREGNANCY; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84885704544     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt277     Document Type: Article

References (72)

1. Angers, S. and Moon, R.T. (2009) Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol., 10, 468-477.
2. Schweizer, L. and Varmus, H. (2003) Wnt/Wingless signaling through beta-catenin requires the function of both LRP/Arrow and frizzled classes of receptors. BMC Cell Biol., 4, 4-15.
3. Veeman, M.T., Axelrod, J.D. and Moon, R.T. (2003) A second canon. Functions and mechanisms of beta-catenin-independentWntsignaling. Dev. Cell, 5, 367-377.
4. Logan, C.Y. and Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol., 20, 781-810.
5. van Amerongen, R. and Nusse, R. (2009) Towards an integrated view of Wnt signaling in development. Development, 136, 3205-3214.
6. MacDonald, B.T., Tamai, K. and He, X. (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell, 17, 9-26.
7. Gordon, M.D. and Nusse, R. (2006) Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J. Biol. Chem., 281, 22429-22433.
8. Ho, H.Y., Susman, M.W., Bikoff, J.B., Ryu, Y.K., Jonas, A.M., Hu, L., Kuruvilla, R. and Greenberg, M.E. (2012) Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc. Natl Acad. Sci. USA, 109, 4044-4051.
9. Clark, C.E., Nourse, C.C. and Cooper, H.M. (2012) The tangled web of non-canonical Wnt signalling in neural migration. Neuro-Signals, 20, 202-220.
10. 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.
11. Kilian, B., Mansukoski, H., Barbosa, F.C., Ulrich, F., Tada, M. and Heisenberg, C.P. (2003) The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev., 120, 467-476.
12. Penzo-Mendez, A., Umbhauer, M., Djiane, A., Boucaut, J.C. and Riou, J.F. (2003) Activation of Gbetagamma signaling downstream of Wnt-11/Xfz7 regulates Cdc42 activity during Xenopus gastrulation. Dev. Biol., 257, 302-314.
13. 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.
14. Greene, N.D. and Copp, A.J. (2009) Development of the vertebrate central nervous system: formation of the neural tube. Prenat. Diagn., 29, 303-311.
15. Wang, Y., Guo, N. and Nathans, J. (2006)The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci., 26, 2147-2156.
16. Hamblet, N.S., Lijam, N., Ruiz-Lozano, P., Wang, J., Yang, Y., Luo, Z., Mei, L., Chien, K.R., Sussman, D.J. andWynshaw-Boris, A. (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development, 129, 5827-5838.
17. 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.
18. Baker, P.C. and Schroeder, T.E. (1967) Cytoplasmic filaments and morphogeneticmovement in the amphibian neural tube. Dev. Biol., 15, 432-450.
19. Freeman, B.G. (1972) Surface modifications of neural epithelial cells during formation of the neural tube in the rat embryo. J. Embryol. Exp. Morphol., 28, 437-448.
20. Schroeder, T.E. (1970) Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. J. Embryol. Exp. Morphol., 23, 427-462.
21. Nishimura, T., Honda, H. and Takeichi, M. (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell, 149, 1084-1097.
22. Ybot-Gonzalez, P., Savery, D., Gerrelli, D., Signore, M., Mitchell, C.E., Faux, C.H., Greene, N.D. and Copp, A.J. (2007) Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development, 134, 789-799.
23. Tahinci, E., Thorne, C.A., Franklin, J.L., Salic, A., Christian, K.M., Lee, L.A., Coffey, R.J. and Lee, E. (2007) Lrp6 is required for convergent extension during Xenopus gastrulation. Development, 134, 4095-4106.
24. Bryja, V., Andersson, E.R., Schambony, A., Esner, M., Bryjova, L., Biris, K.K., Hall, A.C., Kraft, B., Cajanek, L., Yamaguchi, T.P. et al. (2009) The extracellular domain of Lrp5/6 inhibits noncanonical Wnt signaling in vivo. Mol. Biol. Cell, 20, 924-936.
25. Carter, M., Chen, X., Slowinska, B., Minnerath, S., Glickstein, S., Shi, L., Campagne, F., Weinstein, H. and Ross, M.E. (2005) Crooked tail (Cd) model of human folate-responsive neural tube defects is mutated in Wnt coreceptor lipoprotein receptor-related protein 6. Proc. Natl Acad. Sci. USA, 102, 12843-12848.
26. 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.
27. Carter, M., Ulrich, S., Oofuji, Y., Williams, D.A. and Ross, M.E. (1999) Crooked tail (Cd) modelshumanfolate-responsive neural tube defects. Hum. Mol. Genet., 8, 2199-2204.
28. Gray, J.D., Nakouzi, G., Slowinska-Castaldo, B., Dazard, J.E., Sunil Rao, J., Nadeau, J.H. and Elizabeth Ross, M. (2010) Functional interactions between the LRP6 WNT co-receptor and folate supplementation. Hum. Mol. Genet., 19, 4560-4572.
29. Copp, A.J. and Greene, N.D. (2010) Genetics and development of neural tube defects. J. Pathol., 220, 217-230.
30. Miller, R.K. and McCrea, P.D. (2010) Wnt to build a tube: contributions of Wnt signaling to epithelial tubulogenesis. Dev. Dyn., 239, 77-93.
31. Machon, O., van den Bout, C.J., Backman, M., Kemler, R. and Krauss, S. (2003) Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience, 122, 129-143.
32. Zechner, D., Fujita, Y., Hulsken, J., Muller, T., Walther, I., Taketo, M.M., Crenshaw, E.B. 3rd, Birchmeier, W.and Birchmeier, C. (2003) beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol., 258, 406-418.
33. Ulloa, F. and Marti, E. (2010)Wntwonthe war: antagonistic role ofWntover Shh controls dorso-ventral patterning of the vertebrate neural tube. Dev. Dyn., 239, 69-76.
34. Alvarez-Medina, R., Cayuso, J., Okubo, T., Takada, S. and Marti, E. (2008) Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development, 135, 237-247.
35. Yu, W., McDonnell, K., Taketo, M.M. and Bai, C.B. (2008) Wnt signaling determines ventral spinal cord cell fates in a time-dependent manner. Development, 135, 3687-3696.
36. Mohamed, O.A., Clarke, H.J. and Dufort, D. (2004) Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev. Dyn., 231, 416-424.
37. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G.H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002) Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell, 108, 837-847.
38. Copp, A.J. (2005) Neurulation in the cranial region-normal and abnormal. J. Anat., 207, 623-635.
39. Rhee, J.M., Pirity, M.K., Lackan, C.S., Long, J.Z., Kondoh, G., Takeda, J. and Hadjantonakis, A.K. (2006) In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice. Genesis, 44, 202-218.
40. Haigo, S.L., Hildebrand, J.D., Harland, R.M. and Wallingford, J.B. (2003) Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol., 13, 2125-2137.
41. Moore, D.C., Stanisstreet, M. and Evans, G.E. (1987) Morphometric analyses of changes in cell shape in the neuroepithelium of mammalian embryos. J. Anat., 155, 87-99.
42. Eaton, S., Auvinen, P., Luo, L., Jan, Y.N. and Simons, K. (1995) CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol., 131, 151-164.
43. Etienne-Manneville, S. and Hall, A. (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature, 421, 753-756.
44. Etienne-Manneville, S. (2004) Cdc42-the centre of polarity. J. Cell Sci., 117, 1291-1300.
45. Schoenwolf, G.C. and Smith, J.L. (1990) Mechanisms of neurulation: traditional viewpoint and recent advances. Development, 109, 243-270.
46. Kinoshita, N., Sasai, N., Misaki, K. and Yonemura, S. (2008) Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol. Biol. Cell, 19, 2289-2299.
47. Schlessinger, K., Hall, A. and Tolwinski, N. (2009) Wnt signaling pathways meet Rho GTPases. Genes Dev., 23, 265-277.
48. Strutt, D.I., Weber, U. and Mlodzik, M. (1997) The role of RhoA in tissue polarity and Frizzled signalling. Nature, 387, 292-295.
49. Mahaffey, J.P., Grego-Bessa, J., Liem, K.F. Jr and Anderson, K.V. (2013) Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. Development, 140, 1262-1271.
50. Schlessinger, K., McManus, E.J. and Hall, A. (2007) Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J. Cell Biol., 178, 355-361.
51. Khan, Z., Vijayakumar, S., de la Torre, T.V., Rotolo, S. and Bafico, A. (2007) Analysis of endogenousLRP6function reveals a novel feedback mechanism by which Wnt negatively regulates its receptor. Mol. Cell. Biol., 27, 7291-7301.
52. Jung, H., Lee, S.K. and Jho, E.H. (2011) Mest/Peg1 inhibits Wnt signalling through regulation of LRP6 glycosylation. Biochem. J., 436, 263-269.
53. Habas, R., Kato, Y. and He, X. (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell, 107, 843-854.
54. Tanegashima, K., Zhao, H. and Dawid, I.B. (2008) WGEF activates Rho in the Wnt-PCP pathway and controls convergent extension in Xenopus gastrulation. EMBO J., 27, 606-617.
55. Tsuji, T., Ohta, Y., Kanno, Y., Hirose, K., Ohashi, K. and Mizuno, K. (2010) Involvement of p114-RhoGEF and Lfc in Wnt-3a-and dishevelled-induced RhoA activation and neurite retraction in N1E-115 mouse neuroblastoma cells. Mol. Biol. Cell, 21, 3590-3600.
56. Zhu, Y., Tian, Y., Du, J., Hu, Z., Yang, L., Liu, J. and Gu, L. (2012) Dvl2-dependent activation of Daam1 and RhoA regulates Wnt5a-induced breast cancer cell migration. PLoS ONE, 7, e37823-e37835.
57. Ang, S.F., Zhao, Z.S., Lim, L. and Manser, E. (2010) DAAM1 is a formin required for centrosome re-orientation during cell migration. PLoS ONE, 5, e13064-e13074.
58. Hsieh, J.C., Lee, L., Zhang, L., Wefer, S., Brown, K., DeRossi, C., Wines, M.E., Rosenquist, T. and Holdener, B.C. (2003) Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell, 112, 355-367.
59. Greene, N.D., Gerrelli, D., Van Straaten, H.W. and Copp, A.J. (1998) Abnormalities of floor plate, notochord and somite differentiation in the loop-tail (Lp) mouse: a model of severe neural tube defects. Mech. Dev., 73, 59-72.
60. Wallingford, J.B. and Harland, R.M. (2002) Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development, 129, 5815-5825.
61. Sawyer, J.M., Harrell, J.R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M. and Goldstein, B. (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol., 341, 5-19.
62. Rolo, A., Skoglund, P. and Keller, R. (2009) Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev. Biol., 327, 327-338.
63. Gonzalez-Sancho, J.M., Brennan, K.R., Castelo-Soccio, L.A. and Brown, A.M. (2004) Wnt proteins induce dishevelled phosphorylation via an LRP5/6-independent mechanism, irrespective of their ability to stabilize beta-catenin. Mol. Cell. Biol., 24, 4757-4768.
64. Endo, Y., Beauchamp, E., Woods, D., Taylor, W.G., Toretsky, J.A., Uren, A. and Rubin, J.S. (2008) Wnt-3a and Dickkopf-1 stimulate neurite outgrowth in Ewingtumor cells via a Frizzled3-and c-Jun N-terminal kinase-dependent mechanism. Mol. Cell Biol., 28, 2368-2379.
65. 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.
66. Metcalfe, C., Mendoza-Topaz, C., Mieszczanek, J. and Bienz, M. (2010) Stability elements in the LRP6 cytoplasmic tail confer efficient signalling upon DIX-dependent polymerization. J. Cell Sci., 123, 1588-1599.
67. Glickstein, S.B., Monaghan, J.A., Koeller, H.B., Jones, T.K. and Ross, M.E. (2009) Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J. Neurosci., 29, 9614-9624.
68. Lee, C., Scherr, H.M. and Wallingford, J.B. (2007) Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development, 134, 1431-1441.
69. Sudarov, A. and Joyner, A.L. (2007) Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev., 2, 26-47.
70. Mikels, A.J. and Nusse, R. (2006) PurifiedWnt5aprotein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol., 4, e115-e128.
71. Serrano, M., Lin, A.W., McCurrach, M.E., Beach, D. and Lowe, S.W. (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell, 88, 593-602.
72. Gray, J. and Ross, M.E. (2011) Neural tube closure in mouse whole embryo culture. J. Vis. Exp., 56, e3132-e3137.