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The Journal of Neuroscience, August 15, 2001, 21(16):6170-6180
Spatial Shaping of Cochlear Innervation by Temporally Regulated Neurotrophin Expression
Isabel Fariñas1, 2, Kevin R. Jones3, Lino Tessarollo5, Allison J. Vigers3, Eric Huang1, Martina Kirstein2, Dominique C. de Caprona4, Vincenzo Coppola5, Carey Backus1, Louis F. Reichardt1, and Bernd Fritzsch4 1 Program in Neuroscience, Department of Physiology and Howard Hughes Medical Institute, University of California, San Francisco, California 94143-0724, 2 Departamento de Biología Celular, Universidad de Valencia, 46100 Burjassot, Spain, 3 Department of Biology, University of Colorado, Boulder, Colorado 80309, 4 Department of Biomedical Sciences, Creighton University, Omaha, Nebraska 68178, and 5 Neural Development Group, Mouse Cancer Genetics Program, National Cancer Institute, Frederick, Maryland 21701
Previous work suggested qualitatively different effects of neurotrophin 3 (NT-3) in cochlear innervation patterning in different null mutants. We now show that all NT-3 null mutants have a similar phenotype and lose all neurons in the basal turn of the cochlea. To understand these longitudinal deficits in neurotrophin mutants, we have compared the development of the deficit in the NT-3 mutant to the spatial-temporal expression patterns of brain-derived neurotrophic factor (BDNF) and NT-3, using lacZ reporters in each gene and with expression of the specific neurotrophin receptors, trkB and trkC. In the NT-3 mutant, almost normal numbers of spiral ganglion neurons form, but fiber outgrowth to the basal turn is eliminated by embryonic day (E) 13.5. Most neurons are lost between E13.5 and E15.5. During the period preceding apoptosis, NT-3 is expressed in supporting cells, whereas BDNF is expressed mainly in hair cells, which become postmitotic in an apical to basal temporal gradient. During the period of neuronal loss, BDNF is absent from the basal cochlea, accounting for the complete loss of basal turn neurons in the NT-3 mutant. The spatial gradients of neuronal loss in these two mutants appear attributable to spatial-temporal gradients of neurotrophin expression. Our immunocytochemical data show equal expression of their receptors, TrkB and TrkC, in spiral sensory neurons and thus do not relate to the basal turn loss. Mice in which NT-3 was replaced by BDNF show a qualitative normal pattern of innervation at E13.5. This suggests that the pattern of expression of neurotrophins rather than their receptors is essential for the spatial loss of spiral sensory neurons in NT-3 null mutants.
Key words: neurotrophins; ear innervation; development of ear innervation; ear and neurotrophin expression; NT-3; sensory neuron survival
Copyright © 2001 Society for Neuroscience 0270-6474/01/21166170-11$05.00/0
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