Elsevier

Neuroscience

Volume 51, Issue 3, December 1992, Pages 513-532
Neuroscience

Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system

https://doi.org/10.1016/0306-4522(92)90292-AGet rights and content

Abstract

Tyrosine protein kinases trk, trkB and trkC are signal-transducing receptors for the neurotrophins nerve growth factor, brain-derived nerve growth factor, neurotrophin-3 and neurotrophin-4. Here we report on the isolation of cDNA fragments encoding a part of rat trk and irkB proteins, respectively, and characterization of a full-length cDNA clone encoding rat trkC. Cells expressing mRNAs for the different members of the trk family were identified in the rat central nervous system by in situ hybridization using oligonucleotide probes designed from the isolated cDNA sequences and complementary to mRNA sequences coding for the extracellular region of the receptors. The expression of trk mRNA was found to be restricted to neurons of the basal forebrain, caudate-putamen with features of cholinergic cells and to magnocellular neurons of several brainstem nuclei. In contrast, cells expressing trkB and trkC mRNAs were widely distributed in the brain. Areas expressing high levels of trkB or trkC mRNAs included olfactory formations, neocortex, hippocampus, thalamic and hypothalamic nuclei, brainstem nuclei, cerebellum and spinal cord motoneurons. A similar distribution for trkB and trkC mRNAs was shown in most areas but each probe specific for these mRNAs also provided distinct labeling patterns in different subregions, layers and cells.

Comparison between our data and previous analyses of cells expressing mRNAs for neurotrophins and the low-affinity nerve growth factor receptor suggests that different modes of action and different combinations of receptors mediate biological responses to neurotrophins in the adult rat brain.

References (106)

  • DreyfusC.F. et al.

    GABAergic and cholinergic neurons exhibit high-affinity nerve growth factor binding in rat basal forebrain

    Expl Neurol.

    (1989)
  • ErnforsP. et al.

    Developmental and regional expression of β-Nerve Growth Factor receptor mRNA in the chick and rat

    Neuron

    (1988)
  • ErnforsP. et al.

    Expression of nerve growth factor receptor mRNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons

    Neuron

    (1989)
  • ErnforsP. et al.

    Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family

    Neuron

    (1990)
  • FriedmanW.J. et al.

    Temporal and spatial expression of NGF receptor mRNA during postnatal rat brain development analyzed by in situ hybridization

    Brain Res.

    (1991)
  • GageF.H. et al.

    NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum

    Neuron

    (1989)
  • GlassD.J. et al.

    TrkB mediates BNDF/NT-3-dependent survival and proliferation in fibroblast lacking the low affinity NGF receptor

    Cell

    (1991)
  • HallböökF. et al.

    Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary

    Neuron

    (1991)
  • IbanezC. et al.

    Disruption of the low-affinity receptor binding site in nerve growth factor allows neuronal survival and differentiation through binding to the product of the proto-oncogene trk

    Cell

    (1992)
  • JayaramanA.

    Anatomical evidence for cortical projections from the striatum in the cat

    Brain Res.

    (1980)
  • JohnsonD. et al.

    Expression and structure of the human NGF receptor

    Cell

    (1986)
  • KaishoY. et al.

    Cloning and expression of a cDNA encoding a novel human neurotrophic factor

    Fedn Eur. Biochem. Socs. Lett.

    (1990)
  • KissJ. et al.

    Immunohistochemical localization of cells containing nerve growth factor receptor in the different regions of the adult rat forebrain

    Neuroscience

    (1988)
  • KleinR. et al.

    The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain

    Cell

    (1990)
  • KleinR. et al.

    The trk proto-oncogene encodes a receptor for nerve growth factor

    Cell

    (1991)
  • KleinR. et al.

    The trkB tyrosine protein kinase is a receptor for neurotrophin-4

    Neuron

    (1992)
  • KleinR. et al.

    The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3

    Cell

    (1991)
  • KozakM.

    At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells

    J. molec. Biol.

    (1987)
  • LamballeF. et al.

    trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3

    Cell

    (1991)
  • LuB. et al.

    Expression of NGF and NGF receptor mRNA in the developing brain: evidence for local delivery and action of NGF

    Expl Neurol.

    (1989)
  • MaisonpierreP.C. et al.

    NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression

    Neuron

    (1990)
  • MaisonpierreP.C. et al.

    NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression

    Neuron

    (1990)
  • MeakinS.O. et al.

    Molecular investigations on the high-affinity nerve growth factor receptor

    Neuron

    (1991)
  • MesulamM.M. et al.

    Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry

    Neuroscience

    (1984)
  • OppenheimR.W.

    Naturally occurring cell death during neuronal development

    Trends Neurosci.

    (1985)
  • ParentA. et al.

    Acetylcholinesterase-containing neurons in cat pallidal complex: morphological characteristics and projection towards the neocortex

    Brain Res.

    (1981)
  • PioroE.P. et al.

    Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system—I. Forebrain

    Neuroscience

    (1990)
  • PioroE.P. et al.

    Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system—II. Brainstem, cerebellum and spinal cord

    Neuroscience

    (1990)
  • RaivichG. et al.

    The localization and distribution of high affinity nerve growth factor binding sites in the central nervous system of the adult rat. A light microscopic autoradiographic study using125I-nerve growth factor

    Neuroscience

    (1987)
  • RosenthalA. et al.

    Primary structure and biological activity of a novel human neurotrophic factor

    Neuron

    (1990)
  • SchwabM.E. et al.

    Nerve growth factor (NGF) in the rat CNS: absence of specific retrograde axonal transport and tyrosine hydroxylase induction in locus coeruleus and substantia nigra

    Brain Res.

    (1979)
  • SegalM. et al.

    The action of the norepinephrine in the rat hippocampus. II. Activation of the input pathway

    Brain Res.

    (1974)
  • SeilerM. et al.

    Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat

    Brain Res.

    (1984)
  • SoppetD. et al.

    The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor

    Cell

    (1991)
  • SquintoS.O. et al.

    trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not for nerve growth factor

    Cell

    (1991)
  • SutterA. et al.

    Nerve growth factor receptors: characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells

    J. biol. Chem.

    (1979)
  • BanerjeeS.P. et al.

    Binding of nerve growth factor receptor in sympathetic ganglia

  • BardeY.-A. et al.

    Purification of a new neurotrophic factor from mammalian brain

    Eur. molec. biol. Org. J.

    (1982)
  • BatchelorP.E. et al.

    Nerve growth factor receptor and choline acetyltransferase colocalization within the rat forebrain: response to fimbria-fornix transection

    J. comp. Neurol.

    (1989)
  • CeccatelliS. et al.

    Expanded distribution of mRNA for nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in the rat brain after colchicine treatment

  • Cited by (549)

    View all citing articles on Scopus
    *

    Present address: URA-CNRS1200, Laboratoire d'Histologie-Embryologie, Universitéde Bordeaux II, 33076 Bordeaux, France.

    View full text