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The Journal of Neuroscience, May 10, 2006, 26(19):5265-5275; doi:10.1523/JNEUROSCI.4680-05.2006

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Development/Plasticity/Repair
Asymmetric Localization of Vangl2 and Fz3 Indicate Novel Mechanisms for Planar Cell Polarity in Mammals

Mireille Montcouquiol,^1,2 Nathalie Sans,³ David Huss,⁴ Jacob Kach,⁵ J. David Dickman,⁴ Andrew Forge,⁶ Rivka A. Rachel,⁷ Neal G. Copeland,⁷ Nancy A. Jenkins,⁷ Debora Bogani,^8,9 Jennifer Murdoch,⁹ Mark E. Warchol,⁵ Robert J. Wenthold,³ and Matthew W. Kelley¹

¹Section on Developmental Neuroscience, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, Maryland 20892, ²Equipe Avenir 2 "Neurosciences Développementales," Institut F. Magendie des Neurosciences, Institut National de la Santé et de la Recherche Médicale, 33077 Bordeaux Cedex, France, ³Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, Maryland 20892, ⁴Departments of Anatomy and Neurobiology and ⁵Otolaryngology, Washington University School of Medicine, St. Louis, Missouri 63110, ⁶Centre for Auditory Research, UCL Ear Institute, University College London, London WC1X 8EE, United Kingdom, ⁷Mouse Cancer Genetics Program, National Cancer Institute–Frederick, Frederick, Maryland 21702, and ⁸Early Development, Mammalian Genetics Unit, ⁹Medical Research Council, Harwell, Oxfordshire OX11 0RD, United Kingdom

Correspondence should be addressed to Mireille Montcouquiol, Equipe Avenir 2 "Neurosciences Développementales," Institut F. Magendie des Neurosciences, Institut National de la Santé et de la Recherche Médicale, 33077 Bordeaux Cedex, France. Email: montcouquiol{at}bordeaux.inserm.fr

Planar cell polarity (PCP) is a process in which cells develop with uniform orientation within the plane of an epithelium. To begin to elucidate the mechanisms of PCP in vertebrates, the localization of the protein Vangl2 (Van Gogh-like) was determined during the development of the mammalian cochlea. Results indicate that Vangl2 becomes asymmetrically localized to specific cell–cell boundaries along the axis of polarization and that this asymmetry is lost in PCP mutants. In addition, PDZ2 (postsynaptic density/Discs large/zona occludens 1), PDZ3, and PDZ4 of the PCP protein Scrb1 (Scribble) are shown to bind to the C-terminal PDZ binding domain of Vangl2, suggesting that Scrb1 plays a direct role in asymmetric targeting of Vangl2. Finally, Fz3 (Frizzled), a newly demonstrated mediator of PCP, is also asymmetrically localized in a pattern that matches that of Vangl2. The presence and asymmetry of Fz3 at the membrane is shown to be dependent on Vangl2. This result suggests a role for Vangl2 in the targeting or anchoring of Fz3, a hypothesis strengthened by the existence of a physical interaction between the two proteins. Together, our data support the idea that protein asymmetry plays an important role in the development of PCP, but the colocalization and interaction of Fz3 and Vangl2 suggests that novel PCP mechanisms exist in vertebrates.

Key words: inner ear; stereociliary bundle; mechanosensory hair cell; cochlea; Van Gogh; Frizzled; planar polarity

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Received Nov. 1, 2005; revised March 22, 2006; accepted March 25, 2006.

Correspondence should be addressed to Mireille Montcouquiol, Equipe Avenir 2 "Neurosciences Développementales," Institut F. Magendie des Neurosciences, Institut National de la Santé et de la Recherche Médicale, 33077 Bordeaux Cedex, France. Email: montcouquiol{at}bordeaux.inserm.fr

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