Research report
Synaptophysin and Gap-43 proteins in efferent fibers of the inner ear during postnatal development

https://doi.org/10.1016/0165-3806(95)00113-RGet rights and content

Abstract

A rearrangement of afferent and efferent fibers occurs in the postnatal development of the inner ear. Growth and synaptogenesis was explored during this critical period by immunohistochemically monitoring the expression of GAP-43 and synaptophysin. Both proteins were colocalized in efferent fibers beyond postnatal day 3 (pn3). Two distinct synaptophysin- and GAP-43-positive fibers innervated different parts of inner hair cells in the first and second postnatal weeks, respectively. GAP-43-positive efferents projecting to outer hair cells upregulated synaptophysin with base to apex gradient between postnatal day 5 and postnatal day 14. In efferents projecting to outer hair cells GAP-43 was downregulated about 6 days beyond synaptogenesis. In efferents projecting to inner hair cells, however, GAP-43 remained upregulated even beyond pn18, indicating continuous synapse replacement of this fiber type. Both proteins thus improved as excellent markers for growth and synaptogenesis of distinct postnatal efferent fibers.

References (82)

  • R.A. Altschuler et al.

    Enkephalin-like immunoreactivity in the guinea pig organ of Corti: ultrastructural and lesion studies

    Hearing Res.

    (1984)
  • M. Anniko et al.

    Localization of the integral membrane glycoprotein synaptophysin and the surface glycoprotein Egp-34 in the embryonic and adult human inner ear

    J. ORL Relat. Spec.

    (1989)
  • V. Baekelandt et al.

    Alterations in GAP-43 and synapsin immunoreactivity provide evidence for synaptic reorganization in adult cat dorsal lateral geniculate nucleus following retinal lesions

    Eur. J. Neurosci.

    (1994)
  • L.I. Benowitz et al.

    A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism and synaptic plasticity

    Trends Neurosci.

    (1987)
  • L.I. Benowitz et al.

    The relationship of GAP-43 to the development and plasticity of synaptic connections

    Ann. NY Acad. Sci.

    (1991)
  • A.M. Berglund et al.

    Hair cell innervation by spiral ganglion neurons in the mouse

    J. Comp. Neurol.

    (1987)
  • P.J. Coggins et al.

    Biochemistry and functional neurochemistry of a neuronspecific phosphoprotein

    J. Neurochem.

    (1991)
  • D.E. Crowley et al.

    Development of cochlear function in the ear of the infant rat

    J. Comp. Physiol. Psychol.

    (1966)
  • P. De Camilli et al.

    The synaptic vesicle proteins synapsin I and synaptophysin (protein 38) are concentrated both in efferent and afferent nerve endings of the skeletal muscle

    J. Neurosci.

    (1988)
  • S.M. De la Monte et al.

    GAP-43 gene expression during development: persistence in a distinctive set of neurons in the mature central nervous system

    Dev. Brain Res.

    (1989)
  • G. Despres et al.

    Immunohistochemical localization of nerve growth factor receptor in the cochlea and in the brainstem of the perinatal rat

    Hearing Res.

    (1991)
  • S.H. Devoto et al.

    SVP38: a synaptic vesicle protein whose appearance correlates closely with synaptogenesis in the rat nervous system

    Ann. NY Acad. Sci.

    (1986)
  • D. Dirks

    Perception of dichotic and monaural verbal material and cerebral dominance in speech

    Acta Otolaryngol.

    (1964)
  • S.M. Echteler

    Developmental segregation in the afferent projections to mammalian auditory hair cells

  • A.B. Elgoyhen et al.

    α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells

    Cell

    (1994)
  • M.R. Emmerling et al.

    Differential distribution of cholinergic enzymes in the developing mouse cochlea

  • M.R. Emmerling et al.

    Development of acetylcholinesterase in the organ of Corti in vivo and in vitro

    Abstr. J. Int. Soc. Dev. Neurosci.

    (1986)
  • M.R. Emmerling et al.

    Biochemical and morphological differentiation of acetylcholinesterase-positive efferent fibers in the mouse cochlea

    J. Electron. Microsc. Tech.

    (1990)
  • M. Eybalin et al.

    Immunoelectron microscopy identifies several types of GABA-containing efferent synapses in the guinea pig organ of Corti

    Neuroscience

    (1988)
  • M. Fitzgerald et al.

    Gap-43 expression in the developing rat lumbar spiral cord

    Neuroscience

    (1991)
  • P. Gil-Loyzaga et al.

    Synaptophysin in the developing cochlea

    Int. J. Dev. Neurosci.

    (1988)
  • J. Guinan et al.

    Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex

    J. Comp. Neurol.

    (1983)
  • A. Hafidi et al.

    First appearance of type II neurons during ontogenesis in the spiral ganglion of the rat. An immunocytochemical study

    Dev. Brain Res.

    (1989)
  • R.I. Hume et al.

    Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes

    Nature

    (1983)
  • M. Ichikawa et al.

    Expression of synaptophysin during synapse formation between dissociated cortical neurons

    Neurosci. Res.

    (1991)
  • R.D. Jacobson et al.

    A protein associated with axonal growth, GAP-43, is widely distributed and developmental regulated in rat CNS

    J. Neurosci.

    (1986)
  • R. Jahn et al.

    A 38000 dalton membrane protein (p38) present in synaptic vesicles

  • K. Kalil et al.

    Elevated synthesis of an axonally transported protein correlates with axonal outgrowth in normal and injured pyramidal tracts

    J. Neurosci.

    (1986)
  • N.Y.S. Kiang et al.

    Hair cell innervation by spiral ganglion cells in adult cat

    Science

    (1982)
  • N.Y.S. Kiang et al.

    Afferent innervation of the mammalian cochlea

  • K. Kikuchi et al.

    The development of the organ of Corti in the mouse

    Acta Otolaryngol. (Stockh.)

    (1965)
  • P. Knaus et al.

    Expression of synaptophysin during postnatal development of the mouse brain

    J. Neurochem.

    (1986)
  • J.J. Lan et al.

    Neurotrophic differentiation results in reduced levels and altered distribution of synaptophysin in PC 12 cells

    J. Neurochem.

    (1993)
  • P.S. Lasiter et al.

    Postnatal development of protein P-38 (synaptophysin) immunoreactivity in pontine and medullary gustatory zones of rat

    Dev. Brain Res.

    (1989)
  • N. LeClerc et al.

    Synaptophysin expression during synaptogenesis in the rat cerebellar cortex

    J. Comp. Neurol.

    (1989)
  • M. Lenoir et al.

    Cochlear receptor development in the rat with emphasis on synaptogenesis

    Anat. Embryol.

    (1980)
  • M.C. Liberman et al.

    Physiology and anatomy of single olivocochlear neurons in the cat

    Hearing Res.

    (1986)
  • M.C. Liberman et al.

    Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy

    J. Comp. Neurol.

    (1990)
  • J.W. Mandell et al.

    Process outgrowth and synaptic variocosity formation by adult photoreceptors in vitro

    J. Neurosci.

    (1993)
  • T. Matsusaku

    Lamellar bodies in the synaptic cytoplasm of the accessory cone from the chick retina as revealed by electron microscopy

    J. Ultrastruct. Res.

    (1967)
  • C.B. McGuire et al.

    Light-microscopic immunolocalization of the growth associated protein GAP-43 in the developing brain

    Dev. Brain Res.

    (1988)
  • Cited by (0)

    1

    Current address: Biochemistry, Hearing Research Centre, HNO Tübingen, Röntgenweg 11, 72076 Tübingen, Germany.

    View full text