Noncanonical Wnt signaling and neural polarity

Annual Review of Neuroscience

Volumn 29, Issue , 2006, Pages 363-386

  Montcouquiol, Mireille ^a,d   Crenshaw III, E Bryan ^b,c   Kelley, Matthew W ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d INSTITUT FRANÇOIS MAGENDIE   (France)

Author keywords

Convergent extension; Gastrulation; Inner ear; Mechanosensory hair cell; Migration; Neurulation; Planar cell polarity

Indexed keywords

BETA CATENIN; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C; WNT PROTEIN;

CELL MATURATION; CELL MIGRATION; CELL POLARITY; DROSOPHILA; EPITHELIUM; GASTRULATION; GENE ISOLATION; HUMAN; INNER EAR; MORPHOGENESIS; NERVE CELL; NERVOUS SYSTEM; NEURAL TUBE; NEURULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; CELL POLARITY; MODELS, BIOLOGICAL; MORPHOGENESIS; NEURONS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 33748362173     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.29.051605.112933     Document Type: Review

References (106)

1. Ahumada A, Slusarski DC, Liu X, Moon RT, Malbon CC, Wang HY. 2002. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298:2006-10
2. Amonlirdviman S, Khare NA, Tree DR, Chen WS, Axelrod JD, Tomlin CJ. 2005. Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 307:423-26
3. Arimura N, Kaibuchi K. 2005. Key regulators in neuronal polarity. Neuron 48:881-84
4. Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N. 1998. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12:2610-22
5. Axelrod JD. 2001. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 15:1182-87
6. Bilder D, Perrimon N. 2000. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676-80
7. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, et al. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638-42
8. Bingham S, Higashijima S, Okamoto H, Chandrasekhar A. 2002. The Zebrafish trilobite gene is essential for tangential migration of branchiomotor neurons. Dev. Biol. 242:149-60
9. Boutros M, Paricio N, Strutt DI, Mlodzik M. 1998. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94:109-18
10. Bryant J, Goodyear RJ, Richardson GP. 2002. Sensory organ development in the inner ear: molecular and cellular mechanisms. Br. Med. Bull. 63:39-57
11. Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. 2003. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130:4037-46
12. Chen P, Johnson JE, Zoghbi HY, Segil N. 2002. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495-505
13. Chen P, Segil N. 1999. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-90
14. Choi SC, Han JK. 2002. Xenopus Cdc42 regulates convergent extension movements during gastrulation through Wnt/Ca2+ signaling pathway. Dev. Biol. 244:342-57
15. Ciani L, Salinas PC. 2005. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 6:351-62
16. Cotanche DA, Corwin JT. 1991. Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hear. Res. 52:379-402
17. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, et al. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13:1129-33
18. Dabdoub A, Donohue MJ, Brennan A, Wolf V, Montcouquiol M, et al. 2003. Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130:2375-84
19. Darken RS, Scola AM, Rakeman AS, Das G, Mlodzik M, Wilson PA. 2002. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J. 21:976-85
20. Davies A, Formstone C, Mason I, Lewis J. 2005. Planar polarity of hair cells in the chick inner ear is correlated with polarized distribution of c-flamingo-1 protein. Dev. Dyn. 233:998-1005
21. De Calisto J, Araya C, Marchant L, Riaz CF, Mayor R. 2005. Essential role of noncanonical Wnt signaling in neural crest migration. Development 132:2587-97
22. Denman-Johnson K, Forge A. 1999. Establishment of hair bundle polarity and orientation in the developing vestibular system of the mouse. J. Neurocytol. 28:821-35
23. Detrait ER, George TM, Etchevers HC, Gilbert JR, Vekemans M, Speer MC. 2005. Human neural tube defects: developmental biology, epidemiology, and genetics. Neurotoxicol. Teratol. 27:515-24
24. Djiane A, Riou J, Umbhauer M, Boucaut J, Shi D. 2000. Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127:3091-100
25. Du SJ, Purcell SM, Christian JL, McGrew LL, Moon RT. 1995. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol. Cell Biol. 15:2625-34
26. Fanto M, McNeill H. 2004. Planar polarity from flies to vertebrates. J. Cell Sci. 117:527-33
27. Glinka A, Wu W, Onichtchouk D, Blumenstock C, Niehrs C. 1997. Head induction by simultaneous repression of Bmp and Wnt signaling in Xenopus. Nature 389:517-19
28. Goto T, Keller R. 2002. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev. Biol. 247:165-81
29. Guo N, Hawkins C, Nathans J. 2004. Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. USA 101:9277-81
30. Habas R, Kato Y, He X. 2001. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107:843-54
31. Habas R, Dawid IB, He X. 2003. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17:295-309
32. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, et al. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:76-81
33. Huang HC, Klein PS. 2004. The Frizzled family: receptors for multiple signal transduction pathways. Genome Biol. 5:234.1-234-.7
34. Itoh K, Krupnik VE, Sokol SY. 1998. Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and beta-catenin. Curr. Biol. 8:591-94
35. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, et al. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr. Biol. 9:207-10
36. Ille F, Sommer L. 2005. Wnt signaling: multiple functions in neural development. Cell. Mol. Life Sci. 62:1100-8
37. Jenny A, Darken RS, Wilson PA, Mlodzik M. 2003. Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J. 22:4409-20
38. Jessen JR, Topczewski J, Bingham S, Sepich DS, Marlow F, et al. 2002. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4:610-15
39. Keller R. 2002. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298:1950-54
40. Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P. 2001. Ltap/Lpp1, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet. 28:251-55
41. Kishida S, Yamamoto H, Hino S, Ikeda S, Kishida M, Kikuchi A. 1999. DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Mol. Cell. Biol. 19:4414-22
42. Klein TJ, Mlodzik M. 2005. Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell. Dev. Biol. 21:155-76
43. Klingensmith J, Yang Y, Axelrod JD, Beier DR, Perrimon N, Sussman DJ. 1996. Conservation of dishevelled structure and function between flies and mice: isolation and characterization of Dvl2. Mech. Dev. 58:15-26
44. Klingensmith J, Nusse R, Perrimon N. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 8:118-30
45. Kohn AD, Moon RT. 2005. Wnt and calcium signaling: beta-catenin- independent pathways. Cell Calcium 38:439-46
46. Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT. 2000. The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16:279-83
47. Kuhl M. 2002. Non-canonical Wnt signaling in Xenopus: regulation of axis formation and gastrulation. Semin. Cell Dev. Biol. 13:243-49
48. Li L, Yuan H, Xie W, Mao J, Caruso AM, et al. 1999. Dishevelled proteins lead to two signaling pathways. Regulation of LEF-1 and c-Jun N-terminal kinase in mammalian cells. J. Biol. Chem. 274:129-34
49. Liu T, DeCostanzo AJ, Liu X, Wang H, Hallagan S, et al. 2001. G protein signaling from activated rat frizzled-1 to the beta-catenin-Lef-Tcf pathway. Science 292:1718-22
50. Liu Y, Shi J, Lu CC, Wang ZB, Lyuksyutova AI, Song XJ, Zou Y. 2005. Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat. Neurosci. 8:1151-59
51. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781-810
52. Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M. 2004. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93-98
53. Lyuksyutova AI, Lu CC, Milanesio N, King LA, Guo N, et al. 2003. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling, Science 302:1984-88
54. McKenzie E, Krupin A, Kelley MW. 2004. Cellular growth and rearrangement during the development of the mammalian organ of Corti. Dev. Dyn. 229:802-12
55. Mlodzik M. 2002. Planar cell polarization: Do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 18:564-71
56. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW. 2003. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423:173-77
57. Montcouquiol M, Kelley MW. 2003. Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J. Neurosci. 23:9469-78
58. Moon RT, Campbell RM, Christian JL, McGrew LL, Shih J, Fraser S. 1993. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119:97-111
59. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, et al. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391-99
60. Moriguchi T, Kawachi K, Kamakura S, Masuyama N, Yamanaka H, et al. 1999. Distinct domains of mouse dishevelled are responsible for the c-Jun N-terminal kinase/stress-activated protein kinase activation and the axis formation in vertebrates. J. Biol. Chem. 274:30957-62
61. Murdoch JN, Doudney K, Paternotte C, Copp AJ, Stanier P. 2001. Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum. Mol. Genet. 10:2593-601
62. Murdoch JN, Henderson DJ, Doudney K, Gaston-Massuet C, Phillips HM, et al. 2003. Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum. Mol. Genet. 12:87-98
63. Myers DC, Sepich DS, Solnica-Krezel L. 2002. Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? Trends Genet. 18:447-55
64. Nusse R. 2005. Wnt signaling in disease and in development. Cell Res. 15:28-32
65. Park M, Moon RT. 2002. The planar cell-polarity gene stbm regulates cell behavior and cell fate in vertebrate embryos. Nat. Cell. Biol. 4:20-25
66. Penton A, Wodarz A, Nusse R. 2002. A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin. Genetics 161:747-62
67. Perrimon N, Mahowald AP. 1987. Multiple functions of segment polarity genes in Drosophila. Dev. Biol. 119:587-600
68. Peters JM, McKay RM, McKay JP, Graff JM. 1999. Casein kinase I transduces Wnt signals. Nature 401:345-50
69. Rauch GJ, Hammerschmidt M, Blader P, Schauerte HE, Strahle U, et al. 1997. Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb. Symp. Quant. Biol. 62:227-34
70. Rolls MM, Albertson R, Shih HP, Lee CY, Doe CQ. 2003. Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J. Cell. Biol. 163:1089-98
71. Ruben RJ. 1967. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. Suppl. 220:1-44
72. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. 1996. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023-26
73. Sasai N, Nakazawa Y, Haraguchi T, Sasai Y. 2004. The neurotrophin- receptor-related protein NRH1 is essential for convergent extension movements. Nat. Cell Biol. 6:741-48
74. Schwamborn JC, Puschel AW. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7:923-29
75. Sheldahl LC, Park M, Malbon CC, Moon RT. 1999. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9:695-98
76. Sher AE. 1971. The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol. Suppl. 285:1-77
77. Slusarski DC, Yang-Snyder J, Busa WB, Moon RT. 1997. Modulation of embryonic intracellular Ca2+ signaling by Wnt-5A. Dev. Biol. 182:114-20
78. Smalley MJ, Sara E, Paterson H, Naylor S, Cook D, et al. 1999. Interaction of axin and Dvl-2 proteins regulates Dvl-2-stimulated TCF-dependent transcription. EMBO J. 18:2823-35
79. Smith JL, Schoenwolf GC. 1997. Neurulation: coming to closure. Trends Neurosci. 20:510-17
80. Sokol S, Christian JL, Moon RT, Melton DA. 1991. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67:741-52
81. Sussman DJ, Klingensmith J, Salinas P, Adams PS, Nusse R, Perrimon N. 1994. Isolation and characterization of a mouse homolog of the Drosopbila segment polarity gene dishevelled. Dev. Biol. 166:73-86
82. Strutt H, Strutt D. 1999. Polarity determination in the Drosophila eye. Curr. Opin. Genet. Dev. 9:442-46
83. Strutt D. 2003. Frizzled signaling and cell polarisation in Drosophila and vertebrates. Development 130:4501-13
84. Tada M, Smith JC. 2000. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127:2227-38
85. Tada M, Concha ML, Heisenberg CP. 2002. Non-canonical Wnt signaling and regulation of gastrulation movements. Semin. Cell Dev. Biol. 13:251-60
86. Takeuchi M, Nakabayashi J, Sakaguchi T, Yamamoto TS, Takahashi H, et al. 2003. The prickle-related gene in vertebrates is essential for gastrulation cell movements. Curr. Biol. 13:674-79
87. Theisen H, Purcell J, Bennett M, Kansagara D, Syed A, Marsh JL. 1994. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120:347-60
88. Torres MA, Yang-Snyder JA, Purcell SM, DeMarais AA, McGrew LL, Moon RT. 1996. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133:1123-37
89. Tsang M, Lijam N, Yang Y, Beier DR, Wynshaw-Boris A, Sussman DJ. 1996. Isolation and characterization of mouse dishevelled-3. Dev. Dyn. 207:253-62
90. Uemura T, Shimada Y. 2003. Breaking cellular symmetry along planar axes in Drosophila and vertebrates. J. Biochem. (Tokyo) 134:625-30
91. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, et al. 1999. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98:585-95
92. Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. 2003. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13:680-85
93. Wallingford JB. 2005. Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. Am. J. Med. Genet. C Semin. Med. Genet. 135:59-68
94. Wallingford JB, Fraser SE, Harland RM. 2002. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2:695-706
95. Wallingford JB, Harland RM. 2002. Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 129:5815-25
96. Wallingford JB, Rowning BA, Vogeli KM, Rothbacher U, Fraser SE, Harland RM. 2000. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405:81-85
97. Wang HY, Malbon CC. 2003. Wnt signaling, Ca2+, and cyclic GMP: visualizing Frizzled functions. Science 300:1529-30
98. Wang J, Mark S, Zhang X, Qian D, Yoo SJ, et al. 2005. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat. Genet. 37:980-85
99. Wang Y, Thekdi N, Smallwood PM, Macke JP, Nathans J. 2002. Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J. Neurosci. 22:8563-73
100. Wharton KAJ. 2003. Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev. Biol. 253:1-17
101. Wehrli M, Dougan ST, Caldwell K, O'Keefe L, Schwartz S, et al. 2000. Arrow encodes an LDL-receptor-related protein essential for Wingless signaling. Nature 407:527-30
102. Yamamoto H, Kishida S, Kishida M, Ikeda S, Takada S, Kikuchi A. 1999. Phosphorylation of axin, a Wnt signal negative regulator, by glycogen synthase kinase-3beta regulates its stability. J. Biol. Chem. 274:10681-84
103. Yan D, Wallingford JB, Sun TQ, Nelson AM, Sakanaka C, et al. 2001. Cell autonomous regulation of multiple Dishevelled-dependent pathways by mammalian Nkd. Proc. Natl. Acad. Sci. USA 98:3802-7
104. Yanagawa S, van Leeuwen F, Wodarz A, Klingensmith J, Nusse R. 1995. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9:1087-97
105. Yoshida N, Liberman MC. 1999. Stereociliary anomaly in the guinea pig: effects of hair bundle rotation on cochlear sensitivity. Hear. Res. 131:29-38
106. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10:1443-54