Ephrin-A5/EphA4 signalling controls specific afferent targeting to cochlear hair cells

Jean Defourny, Anne-Lise Poirrier, François Lallemend, Susana Mateo Sánchez, Jakob Neef, Pierre Vanderhaeghen, Eduardo Soriano, Christiane Peuckert, Klas Kullander, Bernd Fritzsch, Laurent Nguyen, Gustave Moonen, Tobias Moser and Brigitte Malgrange ()
Additional contact information
Jean Defourny: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36
Anne-Lise Poirrier: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36
François Lallemend: Unit of Molecular Neurobiology, Karolinska Institute
Susana Mateo Sánchez: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36
Jakob Neef: InnerEarLab, University of Göttingen Medical Center
Pierre Vanderhaeghen: Institute of Interdisciplinary Research on Human and Molecular Biology (IRIBHM), Université Libre de Bruxelles (ULB)
Eduardo Soriano: Developmental Neurobiology and Regeneration Unit, Institut de Recerca Biomèdica (IRB) and University of Barcelona, Parc Científic de Barcelona
Christiane Peuckert: Uppsala University, Box 593
Klas Kullander: Uppsala University, Box 593
Bernd Fritzsch: College of Liberal Arts and Sciences, University of Iowa
Laurent Nguyen: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36
Gustave Moonen: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36
Tobias Moser: InnerEarLab, University of Göttingen Medical Center
Brigitte Malgrange: GIGA-Neurosciences, Developmental Neurobiology Unit, University of Liège, C.H.U. B36

Nature Communications, 2013, vol. 4, issue 1, 1-12

Abstract: Abstract Hearing requires an optimal afferent innervation of sensory hair cells by spiral ganglion neurons in the cochlea. Here we report that complementary expression of ephrin-A5 in hair cells and EphA4 receptor among spiral ganglion neuron populations controls the targeting of type I and type II afferent fibres to inner and outer hair cells, respectively. In the absence of ephrin-A5 or EphA4 forward signalling, a subset of type I projections aberrantly overshoot the inner hair cell layer and invade the outer hair cell area. Lack of type I afferent synapses impairs neurotransmission from inner hair cells to the auditory nerve. By contrast, radial shift of type I projections coincides with a gain of presynaptic ribbons that could enhance the afferent signalling from outer hair cells. Ephexin-1, cofilin and myosin light chain kinase act downstream of EphA4 to induce type I spiral ganglion neuron growth cone collapse. Our findings constitute the first identification of an Eph/ephrin-mediated mutual repulsion mechanism responsible for specific sorting of auditory projections in the cochlea.

Date: 2013
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DOI: 10.1038/ncomms2445

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