Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles

Nature Cell Biology

Volumn 10, Issue 11, 2008, Pages 1257-1268

  Devenport, Danelle ^a   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL CONTACT; CELL SHAPE; CYTOSKELETON; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; GENE MUTATION; HAIR FOLLICLE; IN VITRO STUDY; IN VIVO STUDY; MAMMAL; MOLECULAR INTERACTION; MORPHOGENESIS; MOUSE; NONHUMAN; ORIENTATION; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; BODY PATTERNING; CELL POLARITY; CELLS, CULTURED; EMBRYO, MAMMALIAN; EPIDERMIS; FRIZZLED RECEPTORS; GENE EXPRESSION; HAIR; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MORPHOGENESIS; MUTATION; NERVE TISSUE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; TRANSFECTION;

MAMMALIA;

EID: 55549083477     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1784     Document Type: Article

References (50)

1. Zallen, J. A. Planar polarity and tissue morphogenesis. Cell 129, 1051-1063 (2007).
2. Seifert, J. R. & Mlodzik, M. Frizzled/PCP signalling: A conserved mechanism regulating cell polarity and directed motility. Nature Rev. Genet. 8, 126-138 (2007).
3. Jones, C. & Chen, P. Planar cell polarity signaling in vertebrates. Bioessays 29, 120-132 (2007).
4. Kibar, Z. et al. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nature Genet. 28, 25125-5 (2001).
5. Curtin, J. A. et al. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13, 1129-1133 (2003).
6. Montcouquiol, M. et al. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177 (2003).
7. Wang, J. et al. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133, 1767-1778 (2006).
8. Wang, Y., Guo, N. & Nathans, J. 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 (2006).
9. Guo, N., Hawkins, C. & Nathans, J. Frizzled6 controls hair patterning in mice. Proc. Natl Acad. Sci. USA 101, 9277-9281 (2004).
10. Wang, Y., Badea, T. & Nathans, J. Order from disorder: Self-organization in mammalian hair patterning. Proc. Natl Acad. Sci. USA 103, 19800-19805 (2006).
11. Axelrod, J. D. & McNeill, H. Coupling planar cell polarity signaling to morphogenesis. ScientificWorld J. 2, 434-454 (2002).
12. Fuchs, E. Scratching the surface of skin development. Nature 445, 834-842 (2007).
13. Schmidt-Ullrich, R. & Paus, R. Molecular principles of hair follicle induction and morphogenesis. Bioessays 27, 247-261 (2005).
14. Chodankar, R. et al. Shift of localized growth zones contributes to skin appendage morphogenesis: Role of the Wnt/β-catenin pathway. J. Invest. Dermatol. 120, 20-6 (2003).
15. Vaezi, A., Bauer, C., Vasioukhin, V. & Fuchs, E. Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Dev. Cell 3 367-381 (2002).
16. Magerl, M. et al. Patterns of proliferation and apoptosis during murine hair follicle morphogenesis. J. Invest. Dermatol. 116 947-955 (2001).
17. Bitgood, M. J. & McMahon, A. P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138 (1995).
18. Hardy, M. H. & Vielkind, U. Changing patterns of cell adhesion molecules during mouse pelage hair follicle development. 1. Follicle morphogenesis in wild-type mice. Acta Anat. 157, 169-182 (1996).
19. Muller-Rover, S., Peters, E. J., Botchkarev, V. A., Panteleyev, A. & Paus, R. Distinct patterns of NCAM expression are associated with defined stages of murine hair follicle morphogenesis and regression. J. Histochem. Cytochem. 46, 1401-1410 (1998).
20. Harfe, B. D. et al. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118 517-528 (2004).
21. Bastock, R., Strutt, H. & Strutt, D. Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130, 3007-3014 (2003).
22. Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595 (1999).
23. Strutt, D. I. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367-375 (2001).
24. Montcouquiol, M. et al. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell-polarity in Mammals. J. Neurosci. 26, 5265-5275 (2006).
25. Das, G., Reynolds-Kennelly, J. & Mlodzik, M. The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye. Dev. Cell 2, 655-666 (2002).
26. Struff, D., Johnson, R., Cooper, K. & Bray, S. Asymmetric localization of frizzled and the determination of notch-dependent cell fate in the Drosophila eye. Curr. Biol. 12, 813-824 (2002).
27. Bellaiche, Y., Beikudoin-Massiani, O., Stuttem, I. & Schweisguth, F. The planar cell polarity protein Strabismus promotes Pins anterior localization during asymmetric division of sensory organ precursor cells in Drosophila. Development 131, 469-478 (2004).
28. St-Jacques, B. et al. Sonic hedgehog signaling is essential for hair development. Curr. Biol. 8, 1058-1068 (1998).
29. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. & Birchmeier, W. β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545 (2001).
30. Yang, A. et al. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718 (1999).
31. Mills, A. A. et al. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713 (1999).
32. Murdoch, J. N. et al. Circletail, a new mouse mutant with severe neural tube defects: Chromosomal localization and interaction with the loop-tail mutation. Genomics 78, 55-63 (2001).
33. Lawrence, P. A., Struhl, G. & Gasal, J. Planar cell polarity: One or two pathways? Nature Rev. Genet. 8, 555-563 (2007).
34. Taylor, J., Abramova, N., Charlton, J. & Adler, P. N. Van Gogh: A new Drosophila tissue polarity gene. Genetics 150, 199-210 (1998).
35. Adler, P. N., Taylor, J. & Charlton, J. The domineering non-autonomy of frizzled and van Gogh clones in the Drosophila wing is a consequence of a disruption in local signaling. Mech. Dev. 96, 197-207 (2000).
36. Des, G., Jenny, A., Klein, T. J., Eaton, S. & Mlodzik, M. Diego interacts with Prickle and Strabismus/Van Gogh to localize planar cell polarity complexes. Development 131, 4467-4476 (2004).
37. Chen, W. S. et al. Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133, 1093-1105 (2008).
38. Vasioukhin, V., Bauer, C., Yin, M. & Fuchs, E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219 (2000).
39. Lawrence, P. A., Casal, J. & Struhl, G. Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129, 2749-2760 (2002).
40. Heisenberg, C. P. et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 76-81 (2000).
41. Tada, M. & Smith, J. C. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127, 2227-2238 (2000).
42. Qian, D. et al. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306, 121-133 (2007).
43. Reddy, S. et al. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech. Dev. 107, 69-82 (2001).
44. Winter, C. G. et al. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91 (2001).
45. Gho, M. & Schweisguth, F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393, 178-81 (1998).
46. Cooper, M. T. & Bray, S. J. Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397, 526-530 (1999).
47. Tomlinson, A. & Struhl, G. Decoding vectorial information from a gradient: Sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. Development 126, 5725-5738 (1999).
48. Fanto, M. & Mlodzik, M. Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523-526 (1999).
49. Chen, C. W., Jung, H. S., Jiang, T. X. & Chuong, C. M. Asymmetric expression of Notch/Delta/Serrate is associated with the anterior-posterior axis of feather buds. Dev. Biol. 188, 181-187 (1997).
50. Tumbar, T. et al. Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004).