Skip to main content
SpringerLink
Log in

Neurotrophins and TRK Receptors in Hippocampal Development

  • Chapter
Neural Cell Specification

Part of the book series: Altschul Symposia Series ((ALSS,volume 3))

  • 31 Accesses

Abstract

The mammalian nervous system is composed of a large number of differentiated neuronal and glial cell types, which develop from precursor cells during the early development of the brain. Many aspects of the transition of proliferating precursors into differentiated cell types remain elusive because of the complexity of the brain. One way to reduce this complexity is to use in vitro systems to study these developmental steps in a simplified context. This chapter briefly reviews the role of neurotrophins in hippocampal development. The reason for studying the hippocampus is primarily because of its involvement in learning and memory processes as described below. The neurotrophin gene family was chosen because of the widespread distribution of the neurotrophins and their high affinity receptors in the developing and adult hippocampus. This distribution not only suggested previously unidentified hippocampal targets, but it also raised the possibility of autocrine or paracrine as well as target-derived mechanisms of trophic support.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alderson R, Alterman A, Barde Y and Lindsay R (1990): Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5: 297–306.

    Article  PubMed  CAS  Google Scholar 

  • Alema S, Casalbore P, Agostini E and Tato F (1985): Differentiation of PC12 cells induced by v-src oncogene. Nature 316: 557–559.

    Article  PubMed  CAS  Google Scholar 

  • Almazan G and McKay R (1992) An oligodendrocyte precursor cell line from rat optic nerve. Brain Res 579: 234–245.

    Article  PubMed  CAS  Google Scholar 

  • Altman J and Bayer S (1990a): Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301: 325–342.

    Article  CAS  Google Scholar 

  • Altman J and Bayer S (1990b): Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 301: 343–364.

    Article  CAS  Google Scholar 

  • Altman J and Bayer S (1990c): Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301: 365–381.

    Article  CAS  Google Scholar 

  • Altman J and Das G (1965): Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319–336.

    Article  PubMed  CAS  Google Scholar 

  • Alvarez E, Northwood I, Gonzales F, Latour D, Seth A, Abate C, Curran T and Davis R (1991): Pro-Leu-/Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. J Biol Chem 266: 15277–15285.

    PubMed  CAS  Google Scholar 

  • Amaral D and Kurz J (1985): The time of origin of cells demonstrating glutamic acid decarboxylase-like immunoreactivity in the hippocampal formation of the rat. Neurosci Lett 59: 33–39.

    Article  PubMed  CAS  Google Scholar 

  • Ascher P, and Nowak L (1988): Quisqualate and kainate-activated channels in mouse central neurones in culture. J Physiol (Lond) 399: 247–266.

    CAS  Google Scholar 

  • Austin C and Cepko C (1990): Cellular migration patterns in the developing mouse cerebral cortex. Development 110: 713–732.

    PubMed  CAS  Google Scholar 

  • Ayer-LeLievre C, Olson L, Ebendal T, Seiger A and Persson H (1988): Expression of β-nerve growth factor in hippocampal neurons. Science 240: 1339–1441.

    Article  PubMed  CAS  Google Scholar 

  • Bar S and Feramisco J (1985): Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 42: 841–848.

    Article  Google Scholar 

  • Barde Y (1989): Trophic factors and neuronal survival. Neuron 2: 1525–1534.

    Article  PubMed  CAS  Google Scholar 

  • Barde Y, Edgar D and Thoenen H (1982): Purification of a new neurotrophic factor from the mammalian brain. EMBO J 1: 549–553.

    PubMed  CAS  Google Scholar 

  • Bartlett W and Banker G (1984): Electron microscopic studies of axonal and dendritic development by hippocampal neurons in culture. I. Cells which develop without intercellular contacts. J Neurosci 4: 1944–1953.

    PubMed  CAS  Google Scholar 

  • Bartus R, Dean R, Beer B and Lippa A (1982): The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408–417.

    Article  PubMed  CAS  Google Scholar 

  • Bashir Z, Bortolotto Z, Davies C, Berreta N, Irving A, Seal A, Henley J, Jane D, Watkins J and Collingridge G (1993): Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363: 347–350.

    Article  PubMed  CAS  Google Scholar 

  • Bayer S (1980): Development of the hippocampal region in the rat: neurogenesis examined with 3H-Thymidine autoradography. J Comp Neurol 190: 87–114.

    Article  PubMed  CAS  Google Scholar 

  • Bekkers J and Stevens C (1990): Presynaptic mechanisms for longterm potentiation in the hippocampus. Nature 346: 724–729.

    Article  PubMed  CAS  Google Scholar 

  • Berkemeier L, Winslow J, Kaplan D, Nikolics K, Goeddel D and Rosenthal A (1991): Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron 7: 857–866.

    Article  PubMed  CAS  Google Scholar 

  • Birren S and Anderson D (1990): A v-myc-immortalized sympathoadrenal progenitor cell line in which neuronal differentiation is initiated by FGF but not NGF. Neuron 4: 189–201.

    Article  PubMed  CAS  Google Scholar 

  • Birren S, Verdi J and Anderson D (1992): Membrane depolarization induces pl40trk and NGF responsiveness, but not p75LNGFR, in MAH cells. Science 257: 395–397.

    Article  PubMed  CAS  Google Scholar 

  • Blackstad T (1956): Commisural connections of the hippocampal region in the rat with special reference to the mode of termination. J Comp Neurol 105: 417–537.

    Article  PubMed  CAS  Google Scholar 

  • Bliss T and Collingridge G (1993): A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39.

    Article  PubMed  CAS  Google Scholar 

  • Bliss T and Lomo T (1973): Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (London) 232: 331–356.

    CAS  Google Scholar 

  • Blusztajn J, Venturini A, Jackson D, Lee H and Wainer B (1992): Acetylcholine synthesis and release is enhanced by dibutyryl c-AMP in a neuronal cell line derived from mouse septum. J Neurosci 12: 793–799.

    PubMed  CAS  Google Scholar 

  • Bothwell M (1991): Keeping track of the neurotrophin receptors. Cell 65: 915–918.

    Article  PubMed  CAS  Google Scholar 

  • Bottenstein J and Sato G (1979): Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 76: 514–517.

    Article  PubMed  CAS  Google Scholar 

  • Boulton T, Nye S, Robbins D, Ip N, Radziejewska E, Morgenbesser S, DePinho R, Panayotatos N, Cobb M and Yancopoulos G (1991): ERKs: a family of protein serine-threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65: 663–675.

    Article  PubMed  CAS  Google Scholar 

  • Brodai A (1978): Neurological anatomy: In relation to clinical medicine. New York: Oxford University Press.

    Google Scholar 

  • Caeser M and Aertsen A (1991): Morphological organization of rat hippocampal slice cultures. J Comp Neurol 307: 87–106.

    Article  PubMed  CAS  Google Scholar 

  • Carter A and Downes C (1992): Phosphatidylinositol 3-kinase is activated by nerve growth factor and epidermal growth factor in PC12 cells. J Biol Chem 267: 14563–14567.

    PubMed  CAS  Google Scholar 

  • Chao M, Bothwell M, Ross A, Koprowski H, Lanahan A, Buck C and Sehgal A (1986): Gene transfer and molecular cloning of the human NGF receptor. Science 232: 518–521.

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Sarnecki C and Blenis J (1992) Nuclear localization and regulation of erk-and rskencoded protein kinases. Mol Cell Biol 12: 915–927.

    PubMed  CAS  Google Scholar 

  • Cheng B and Mattson M (1991) NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron 7: 1031–1041.

    Article  PubMed  CAS  Google Scholar 

  • Collazo D, Takahashi H and McKay R (1992): Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9: 643–656.

    Article  PubMed  CAS  Google Scholar 

  • Cordon-Cardo C, Tapley P, Jing S, Nanduri V, O’Rourke E, Lamballe F, Kovary K, Klein R, Jones K, Reichardt L and Barbacid M (1991): The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66: 173–183.

    Article  PubMed  CAS  Google Scholar 

  • Dotti C, Sullivan C and Banker G (1988): The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454–1468.

    PubMed  CAS  Google Scholar 

  • Durkop H, Latza U, Hummel M, Eitelbach F, Seed B, and Stein H (1992): Molecular cloning and expression of a new member of the nerve growth factor receptor family that is characteristic for Hodgkin’s disease. Cell 68: 421–427.

    Article  PubMed  CAS  Google Scholar 

  • Ernfors P, Ibanez C, Ebendal T, Olson L and Persson H (1990a): Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression. Proc Natl Acad Sci USA 87: 5454–5458.

    Article  CAS  Google Scholar 

  • Ernfors P, Merlio J and Persson H (1992): Cells expressing mRNAs for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4: 1140–1158.

    Article  PubMed  Google Scholar 

  • Ernfors P, Wetmore C, Olson L and Persson H (1990b): Identification of cells in the rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5: 511–526.

    Article  CAS  Google Scholar 

  • Eves E, Tucker M, Roback J, Downen M, Rich M and Wainer B (1992): Immortal rat hippocampal cell lines exhibit neuronal and glial lineages and neurotrophin gene expression. Proc Natl Acad Sci USA 89: 4373–4377.

    Article  PubMed  CAS  Google Scholar 

  • Frederiksen K and McKay R (1988): Proliferation and differentiation of rat neuroephitelial precursor cells in vivo. J Neurosci 8: 1144–1151.

    PubMed  CAS  Google Scholar 

  • Frederiksen K, Jat P, Valtz N, Levy D and McKay R (1988): Immortalization of precursor cells from the mammalian CNS. Neuron 1: 439–448.

    Article  PubMed  CAS  Google Scholar 

  • Friedman W, Ernfors P and Persson H (1991a): Transient and persistent expression of NT-3/BDNF mRNA in the rat brain during postnatal development. J Neurosci 11: 1577–1584.

    CAS  Google Scholar 

  • Friedman W, Olson L and Persson H (1991b): Cells that express brain-derived neurotrophic factor in the developing postnatal brain. Eur J Neurosci 3: 688–697.

    Article  Google Scholar 

  • Furshpan E and Potter D (1989): Seizure-like activity and cellular damage in rat hippocampal neurons in culture. Neuron 3: 199–207.

    Article  PubMed  CAS  Google Scholar 

  • Galileo D, Gray G, Owens G, Majors J and Sanes J (1990): Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-antibodies. Proc Natl Acad Sci USA 87: 458–462.

    Article  PubMed  CAS  Google Scholar 

  • Gall C and Isackson P (1989): Limbic seizures increase neuronal production of mRNA for nerve growth factor. Science 245: 758–761.

    Article  PubMed  CAS  Google Scholar 

  • Glass D, Nye S, Hantzopoulos P, Macchi M, Squinto S, Goldfarb M and Yancopoulos G (1991): TrkB mediates BDNF/NT-3-dependent survival and proliferation in fibroblasts lacking the low affinity NGF receptor. Cell 66: 405–413.

    Article  PubMed  CAS  Google Scholar 

  • Gray G, Glover J, Majors J and Sanes J (1988): Radial arrangement of clonally related cells in the chicken optic tectum: Lineage analysis with a recombinant retrovirus. Proc Natl Acad Sci USA 85: 7356–7360.

    Article  PubMed  CAS  Google Scholar 

  • Greenberg M, Greene L and Ziff E (1985): Nerve growth factor and epidermal growth factor induce rapid transient changes in proto-oncogene transcription in PC 12 cells. J Biol Chem 260: 14101–14110.

    PubMed  CAS  Google Scholar 

  • Greene L (1976): Establishment of a nonadrenergic clonal line of rat adrenal pheochromocytoma cells which responds to nerve growth factor. Proc Natl Acad Sci USA 73: 2424–2428.

    Article  PubMed  CAS  Google Scholar 

  • Greene L, Shain W, Chalazonitis A, Breakfield X, Minna J, Coon H and Nerenberg M (1975): Neuronal properties of hybrid neuroblastoma X sympathetic ganglion cells. Proc Natl Acad Sci USA 72: 4923–4927.

    Article  PubMed  CAS  Google Scholar 

  • Grove E, Kirkwood T and Price J (1992): Neuronal precursor cells in the rat hippocampal formation contribute to more than one cytoarchitectonic area. Neuron 8: 217–229.

    Article  PubMed  CAS  Google Scholar 

  • Hagag N, Halegoua S and Viola M (1986): Inhibition of growth factor-induced differentiation of PC12 cells by microinjection of antibody to Ras p21. Nature 319: 680–682.

    Article  PubMed  CAS  Google Scholar 

  • Halegoua S, Armstrong R and Kremer N (1991): Dissecting the mode of action of neuronal growth factor. Curr Top Microbiol Immunol 165: 119–170.

    Article  PubMed  CAS  Google Scholar 

  • Hallbook F, CF, I., and Persson, H. (1991). Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6: 845–858.

    Article  PubMed  CAS  Google Scholar 

  • Hama T, Huang K and Guroff G (1986): Protein kinase C is a component of a nerve growth factor sensitive phosphorylation system in PC12 cells. Proc Natl Acad Sci USA 87: 2353–2357.

    Article  Google Scholar 

  • Hamburger V, Brunsco-Bechtold J and Yip J (1981): Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor. J Neurosci 1: 60–71.

    PubMed  CAS  Google Scholar 

  • Hammang J, Baetge E, Behiringer R, Brinster R, Palmiter R and Messing A (1990): Immortalized retinal neurons derived from SV40 T-antigen-induced tumors in transgenic mice. Neuron 4: 775–782.

    Article  PubMed  CAS  Google Scholar 

  • Han H, Nichols R, Rubin M, Bahler M and Greenegard P (1991): Induction of formation of presynaptic terminals in neuroblastoma cells by Synapsin IIb. Nature 349: 697–700.

    Article  PubMed  CAS  Google Scholar 

  • Hanks S (1991): Eucaryotic protein kinases. Current Opin Struct Biol 1: 369–383.

    Article  CAS  Google Scholar 

  • Hanks S, Quinn A and Hunter T (1988): The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52.

    Article  PubMed  CAS  Google Scholar 

  • Hayes T and McKay R (1993): Differentiation Of Cell Types In The Central Nervous System. Wiley-Liss Inc.

    Google Scholar 

  • Hefti F (1986): Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6: 845–858.

    Google Scholar 

  • Hempstead B, Martin-Zanca D, Kaplan D, Parada L and Chao M (1991): High affinity NGF binding requires co-expression of the trk proto-oncogene and the low affinity NGF receptor. Nature 350: 678–683.

    Article  PubMed  CAS  Google Scholar 

  • Hempstead B, Schleifer L and Chao M (1989): Expression of a functional gene for nerve growth factor after gene transfer. Science 243: 373–375.

    Article  PubMed  CAS  Google Scholar 

  • Heuer J, Fatemie-Nainie S, Wheeler E and Bothwell M (1990): Structure and development of the chicken NGF receptor. Dev Biol 137: 287–304.

    Article  PubMed  CAS  Google Scholar 

  • Hirano S, Fuse S and Sohal G (1991): The effect of the floor plate on pattern and polarity in the developing central nervous system. Science, 251, 310–313.

    Article  PubMed  CAS  Google Scholar 

  • Hofer M, Pagliusi S, Hohn A, Leibrock J and Barde Y (1990): Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 9: 2459–2464.

    PubMed  CAS  Google Scholar 

  • Hohn A, Leibrock J, Bailey K and Barde Y (1990): Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 344: 339–341.

    Article  PubMed  CAS  Google Scholar 

  • Holt C, Bertsch T, Ellis H and Harris W (1988): Cellular determination in the Xenopus retina is independent of lineage and birthdate. Neuron 1: 15–26.

    Article  PubMed  CAS  Google Scholar 

  • Hyman C, Hofer M, Barde Y, Juhasz M, Yancopoulos G, Squinto S and Lindsay R (1991): BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350: 230–232.

    Article  PubMed  CAS  Google Scholar 

  • Ibanez C, Ebendal T, Barbany G, Murray-Rust J, Blundell T and Persson H (1992a): Disruption of the low affinity receptor-binding site in NGF allows neuronal survival and differentiation by binding to the trk gene product. Cell 69: 329–341.

    Article  CAS  Google Scholar 

  • Ibanez C, Ebendal T and Persson H (1991): Chimeric molecules with multiple neurotrophic activities reveal structural elements determining the specificities of NGF and BDNF. EMBO J 10: 2105–2110.

    PubMed  CAS  Google Scholar 

  • Ibanez C, Ernfors P, Timmusk T, Ip N, Yancopoulos G and Persson H (1993): Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development 117: 1345–1353..

    PubMed  CAS  Google Scholar 

  • Ibanez C, Ilag L, Murray-Rust J and Persson H (1993): An extended surface of binding to Trk tyrosine kinase receptors in NGF and BDNF allows the engineering of a functional pan-neurotrophin. EMBO J 12: 2281–2293.

    PubMed  CAS  Google Scholar 

  • Ip N, Ibanez C, Nye S, McClain J, Jones P, Gies D, Belluscio L, Le Beau M, Espinosa EI, Squinto S, Persson H and Yancopoulos G (1992): Mammalian Neurotrophin-4: structure, chromosomal localization, tissue distribution and receptor specificity. Proc Natl Acad Aci USA 89: 3060–3064.

    Article  CAS  Google Scholar 

  • Ip N, Li Y, Van de Stadt I, Panayotatos N, Alderson R and Lindsay R (1991): Ciliary neurotrophic factor enhances neuronal survival in embryonic rat hippocampal cultures. J Neurosci 11: 3124–3134.

    PubMed  CAS  Google Scholar 

  • Ip N, Li Y, Yancopoulos G and Lindsay R (1993a): Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13: 3394–3405.

    CAS  Google Scholar 

  • Ip N, Stitt T, Tapley P, Klein R, Glass D, Fandl J, Greene L, Barbacid M and Yancopoulos G (1993b): Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10: 137–149.

    Article  CAS  Google Scholar 

  • Isackson P, Huntsman M, Murray K and Gall C (1991): BDNF mRNA expression is increased in the adult forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6: 937–948.

    Article  PubMed  CAS  Google Scholar 

  • Ithoh N, Yonehara S, Ishii A, Yonehara M, Mizushima S, Sameshima M, Hase A, Seto Y and Nagata S (1991): The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66: 233–243.

    Article  Google Scholar 

  • Jing S, Tapley P and Barbacid M (1992): Nerve growth factor mediates signal transduction through trk homodimer receptors. Neuron 9: 1067–1079.

    Article  PubMed  CAS  Google Scholar 

  • Johnson D, Lanahan A, Buck C, Sehgal A, Morgan C, Mercer E, Bothwell M and Chao M (1986): Expression and structure of the human NGF receptor. Cell 47: 545–554.

    Article  PubMed  CAS  Google Scholar 

  • Jones K and Reichardt L (1990): Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc Natl Acad Sci USA 87: 8060–8064.

    Article  PubMed  CAS  Google Scholar 

  • Kaisho Y, Yoshimura K and Nakahama K (1990): Cloning and expression of a cDNA encoding a novel human neurotrophic factor. FEBS Lett 266: 187–191.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan D, Hempstead B, Martin-Zanca D, Chao M and Parada L (1991a): The trk protooncogene product: a signal transducing receptor for nerve growth factor. Science 252: 554–558.

    Article  CAS  Google Scholar 

  • Kaplan D, Martin-Zanca D and Parada L (1991b): Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350: 158–160.

    Article  CAS  Google Scholar 

  • Kim U, Fink D, Kim H, Park D, Contreras M, Guroff G and Rhee S (1991): Nerve growth factor stimulates phosphorylation of phospholipase C--y in PC 12 cells. J Biol Chem 266: 1359–1362.

    PubMed  CAS  Google Scholar 

  • Klee W and Nerenberg M (1974): A neuroblastoma X glioma hybrid cell line with morphine receptors. Proc Natl Acad Sci USA 69: 3474–3477.

    Article  Google Scholar 

  • Klein R, Conway D, Parada L and Barbacid M (1990): The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the tyrosine kinase domain. Cell 61: 647–656.

    Article  PubMed  CAS  Google Scholar 

  • Klein R, Nanduri V, Jing S, Lamballe FPT, Bryant S, Cordon-Cardo C, Jones K, Reichardt L and Barbacid M (1991a): The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophin factor and neurotrophin-3. Cell 66: 395–403.

    Article  CAS  Google Scholar 

  • Klein R, Jing S, Nanduri V, O’Rourke E and Barbacid M (1991b): The trk protooncogene encodes a receptor for nerve growth factor. Cell 65: 189–197.

    Article  CAS  Google Scholar 

  • Knusel B, Winslow J, Rosenthal A, Burton L, Seid D, Nikolics K and Hefti F (1991): Promotion of central cholinergie and dopaminergic differentiation by brain-derived neurotrophic factor but not neurotrophin-3. Proc Natl Acad Sci USA 88: 961–965.

    Article  PubMed  CAS  Google Scholar 

  • Koch C, Anderson D, Moran M, Ellis C and Pawson T (1991): SH2 and SH3 domains: Elements that control interactions of cytoplasmic signaling proteins. Science 252: 668–674.

    Article  PubMed  CAS  Google Scholar 

  • Kremer N, D’Arcangelo G, Thomas S, DeMarco M, Brugge J and Halegoua S (1991): Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of Src and Ras actions. J Cell Biol 115: 809–819.

    Article  PubMed  CAS  Google Scholar 

  • Lamballe F, Klein R and Barbacid M (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66: 967–979.

    Article  PubMed  CAS  Google Scholar 

  • Lamballe F, Smeyne R and Barbacid M (1994): Developmental expression of trkC, the Neurotrophin-3 receptor, in the mammalian nervous system. J Neurosci 14: 14–28.

    PubMed  CAS  Google Scholar 

  • Land H, Parada L and Weinberg R (1983): Tumorigenic conversion of primary embryo fibroblast requires at least two cooperating oncogenes. Nature 304: 596–602.

    Article  PubMed  CAS  Google Scholar 

  • Lander A (1987): Molecules that make axons grow. Mol Neurobiol 1: 213–245.

    Article  PubMed  CAS  Google Scholar 

  • Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H and Barde Y (1989): Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341: 149–152.

    Article  PubMed  CAS  Google Scholar 

  • Lendahl U, Zimmerman L and McKay R (1990): CNS stem cells express a new class of intermediate filament proteins. Cell 60: 585–595.

    Article  PubMed  CAS  Google Scholar 

  • Levi-Montalcini R (1987): The nerve growth factor: thirty-five years later. Science 237: 1154–1162.

    Article  PubMed  CAS  Google Scholar 

  • Li B, Kaplan D, Kung H and Kamata T (1992): Nerve growth factor stimulation of Ras-guanine nucleotide exchange factor and GAP activities. Science 256: 1456–1459.

    Article  PubMed  CAS  Google Scholar 

  • Lindsay R, Thoenen H and Barde Y (1985): Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev Biol 112: 319–328.

    Article  PubMed  CAS  Google Scholar 

  • Loeb D, Maragos J, Martin-Zanca D, Chao M, Parada L and Greene L (1991): The trk proto-oncogene rescues NGF responsiveness in mutant NGF-nonresponsive PC 12 cell lines. Cell 66: 961–966.

    Article  PubMed  CAS  Google Scholar 

  • Lorente de Nó R (1934): Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46: 113–177.

    Google Scholar 

  • Maher P (1988): Nerve growth factor induces protein-tyrosine phosphorylation. Proc Natl Acad Sci USA 85: 6788–6791.

    Article  CAS  Google Scholar 

  • Maisonpierre P, Belluscio L, Friedman B, Alderson R, Wiegand S, Furth M, Lindsay R and Yancopoulos G (1990a): NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5: 501–509.

    Article  CAS  Google Scholar 

  • Maisonpierre P, Belluscio L, Squinto S, Ip N, Furth M, Lindsay R and Yancopoulos G (1990b): Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247: 1446–1451.

    Article  CAS  Google Scholar 

  • Malinow R and Tsien R (1990): Presynsaptic enhancement shown by whole cell recordings of long-term potentiation in hippocampal slices. Nature 346: 177–180.

    Article  PubMed  CAS  Google Scholar 

  • Mallet S and Barclay A (1991): A new superfamily of cell surface proteins related to nerve growth factor receptor. Immunol. Today 12: 220–223.

    Google Scholar 

  • Manabe T, Renner P and Nicoll R (1992): Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355: 50–55.

    Article  PubMed  CAS  Google Scholar 

  • Martin-Zanca D, Hughes S and Barbacid M (1986): A human oncogene formed by the fusion of truncated tropomyosin and protein kinase sequences. Nature 319: 743–748.

    Article  PubMed  CAS  Google Scholar 

  • Martin-Zanca D, Oskam R, Mitra G, Copeland T and Barbacid M (1989): Molecular and biochemical characterization of the human trk protooncogene. Molec Cell Biol 1989: 24–33.

    Google Scholar 

  • Mattson M, and Kater S (1989): Development and selective neurodeneration in cells cultured from different hippocampal regions. Brain Res 490: 110–125.

    Article  PubMed  CAS  Google Scholar 

  • Mattson M and Rychlik B (1990): Glia protect hippocampal neurons against excitatory amino acid-induced degeneration: involvement of fibroblast growth factor. Int J Dev Neurosci 8: 399–416.

    Article  PubMed  CAS  Google Scholar 

  • McConnell S (1988): Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J Neurosci 8: 945–974.

    PubMed  CAS  Google Scholar 

  • McConnell S and Kaznowski C (1991): Cell cycle dependence of laminar determination in developing neocortex. Science 254: 282–285.

    Article  PubMed  CAS  Google Scholar 

  • McDonald N, Lapatto R, Murray R, Gunning J, Wlodawer A and Blundell T (1991): New protein fold revealed by a 2.3 Å resolution crystal structure of nerve growth factor. Nature 354: 411–414.

    Article  PubMed  CAS  Google Scholar 

  • Meakin S and Shooter E (1991): Molecular investigations on the high-affinity nerve growth factor receptor. Neuron 6: 153–163.

    Article  PubMed  CAS  Google Scholar 

  • Mellon P, Windle J, Goldsmith P, Padola C, Roberts J and Weiner R (1990): Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5: 1–10.

    Article  PubMed  CAS  Google Scholar 

  • Merlio J, Ernfors P, Jaber M and Persson H (1993): Molecular cloning of rat trkC and identification of cells expressing mRNAs for members of the trk family in the rat Central Nervous System. Neurosci 51: 513–532.

    Article  Google Scholar 

  • Merlio J, Ernfors P, Kokaia Z, Middlemas D, Bengzon J, Kokaia M, Smith M, Siesjo B, Hunter T, Lindvall O and Persson H (1993): Increased production and activation of the tyrosine kinase receptor trkB after brain insults. Neuron 10: 151–164.

    Article  PubMed  CAS  Google Scholar 

  • Middlemas D, Lindberg R and Hunter T (1991): trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 11: 143–153.

    PubMed  CAS  Google Scholar 

  • Milbrandt J (1987): Nerve growth factor induced gene encodes a possible transcription regulatory factor. Science 238: 797–799.

    Article  PubMed  CAS  Google Scholar 

  • Milbrandt J (1988): Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1: 183–188.

    Article  PubMed  CAS  Google Scholar 

  • Morris R, Davis S and Butcher S (1990): Hippocampal synaptic plasticity and NMDA receptors: a role in information storage. Phil.Trans R. Soc 329: 187–204.

    Article  CAS  Google Scholar 

  • Nakielny S, Cohen P, Wu J and Sturgill T (1992): MAP kinase activator from insulin-stimulated skeletal muscle is a protein threonine/tyrosine kinase. EMBO J 11: 2123–2129.

    PubMed  CAS  Google Scholar 

  • Noda M, Ko M, Ogura A, Liu D, Amano T, Takano T and Ikawa Y (1985): Sarcoma viruses carrying the ras oncogene induce differentiation-associated properties in a neuronal cell line. Nature 318: 73–75.

    Article  PubMed  CAS  Google Scholar 

  • Ohmichi M, Decker S and Saltiel A (1992a): Activation of phosphatidylinositol-3 kinase by nerve growth factor involves indirect coupling of the trk proto-oncogene with src homology 2 domains. Neuron 9: 769–777.

    Article  CAS  Google Scholar 

  • Ohmichi M, Pang L, Decker S and Saltiel A (1992b): Nerve growth factor stimulates the activities of the Raf-1 and the mitogen-activated protein kinases via the trk protooncogene. J Biol Chem 267: 14604–14610.

    CAS  Google Scholar 

  • Phillips H, Hains J, Laramee G, Rosenthal A and Winslow J (1990): Widespread expression of BDNF but not NT-3 by target areas of basal forebrain cholinergic neurons. Science 250: 290–294.

    Article  PubMed  CAS  Google Scholar 

  • Price J and Thurlow L (1988): Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104: 473–482.

    PubMed  CAS  Google Scholar 

  • Pulver B, Kyriakis J, Avruch J, Nikolakaki E and Woodget J (1991): Phosphorylation of c-Jun mediated by Map kinases. Nature 353: 670–674.

    Article  Google Scholar 

  • Purves D (1988): “A Molecular Basis For Trophic Interactions In Vertebrates” Cambridge, Massachusetts: Harvard University Press.

    Google Scholar 

  • Radeke M, Misko T, Hsu C, Herzenberg L and Shooter E (1987): Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 9: 593–597.

    Article  Google Scholar 

  • Rakic P (1988): Specification of cerebral cortical areas. Science 241: 170–176.

    Article  PubMed  CAS  Google Scholar 

  • Ramón y Cajal S (1990): “New Ideas On The Structure Of The Nervous System In Man And Vertebrates” 1st Edition (Swanson N, Swanson LW Trans.) Cambridge, MA: MIT Press.

    Google Scholar 

  • Renfranz P, Cunningham M and McKay R (1991): Region-specific differentiation of the hippocampal stem cell line HiB5 upon transplantation into the developing mammalian brain. Cell 66: 713–729.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Tebar A, Dechant G, Gotz R and Barde Y (1992): Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO J 11: 917–922.

    PubMed  CAS  Google Scholar 

  • Rohrer H, Hofer M, Hellweg R, Korsching S, Stehle A, Saadat S and Thoenen H (1988): Antibodies against mouse nerve growth factor interfere in vivo with the development of avian sensory and sympathetic neurons. Development 103: 545–552.

    PubMed  CAS  Google Scholar 

  • Rosenthal A, Goeddel D, Nguyen T, Lewis M, Shih A, Laramee G, Nikolics K and Winslow J (1990): Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4: 767–773.

    Article  PubMed  CAS  Google Scholar 

  • Rozakis-Adcock A, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci P, Schlessinger J and Pawson T (1992): Association of SHC and GRB2/sem-5 SH2 containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360: 689–692.

    Article  PubMed  CAS  Google Scholar 

  • Rozenberg F, Robain O, Jardin L and Ben-Ari Y (1989): Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Dev Brain Res 50: 177–187.

    Article  CAS  Google Scholar 

  • Ruley H (1983): Adenovirus early region lA enables viral and cellular transforming genes to transform primary cells in culture. Nature 304: 602–606.

    Article  PubMed  CAS  Google Scholar 

  • Ryder E, Snyder E and Cepko C (1990): Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J Neurobiol 21: 356–375.

    Article  PubMed  CAS  Google Scholar 

  • Schlessinger J and Ullrich A (1992): Growth factor signaling by receptor tyrosine kinases. Cell 9: 383–391.

    CAS  Google Scholar 

  • Silva A, Paylor R, Wehner J and Tonegawa S (1992b): Impaired spatial learning in aCalcium-Calmodulin Kinase II Mutant Mice. Science 257: 206–211.

    Article  CAS  Google Scholar 

  • Silva A, Stevens C, Tonegawa S and Wang Y (1992a): Deficient hippocampal long-term potentiation in a-Calcium-Calmodulin Kinase II mutant mice. Science 257: 201–205.

    Article  CAS  Google Scholar 

  • Snyder E, Deitcher D, Walsh C, Arnold-Aldea S, Hartwieg E and Cepko C (1992): Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 68: 33–51.

    Article  PubMed  CAS  Google Scholar 

  • Soltoff S, Rabin S, Cantley L and Kaplan D (1992): Nerve growth factor promotes the activation of phosphatidylinositol 3-kinase and its association with the trk tyrosine kinase. J Biol Chem 267: 17472–17477.

    PubMed  CAS  Google Scholar 

  • Soppet D, Escandon E, Maragos J, Middlemas D, Reid S, Blair J, Burton L, Stanton B, Kaplan D, Hunter T, Nikolics K and Parada L. (1991): The neurotrophic factor brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65: 895–903.

    Article  PubMed  CAS  Google Scholar 

  • Spemann, H. (1938). “Embryonic development and induction”. New Haven, Conn.: Yale University Press.

    Book  Google Scholar 

  • Stoppin L, Buchs P and Muller D (1991): A simplified method for organotypic cultures of nervous tissue. J Neurosci Meth 37: 173–182.

    Article  Google Scholar 

  • Swanson L and Cowan W (1977): An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 17: 49–84.

    Article  Google Scholar 

  • Temple S (1989): Division and differentiation of isolated CNS blast cells in microculture. Nature 340: 471–473.

    Article  PubMed  CAS  Google Scholar 

  • Tessarollo L, Tsoulfas P, Martin-Zanca D, Gilbert D, Jenkins N, Copeland N and Parada L (1993): trkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development 118: 463–475.

    PubMed  CAS  Google Scholar 

  • Tessier-Lavigne M, Placzek M and Lumsden A (1988): Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336: 775–778.

    Article  PubMed  CAS  Google Scholar 

  • Thomas G (1992): MAP kinase by any other name smells just as sweet. Cell 68: 3–6.

    Article  PubMed  CAS  Google Scholar 

  • Timmusk T, Belluardo N, Metsis M and Persson H (1993a): Widespread and developmentally regulated expression of Neurotrophin-4 in rat brain and peripheral tissues. Eur. J. Neurosci., 5, 605–613.

    Article  CAS  Google Scholar 

  • Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M and Persson H (1993b): Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10: 475–489.

    Article  CAS  Google Scholar 

  • Troppmair J, Bruder J, App H, Cai H, Liptak L, Szeberenyl J, Cooper G and Rapp U (1992): Ras controls coupling of growth factor receptors Protein Kinase C in the membrane to Raf-1 and B-Raf protein serine kinases in the cytosol. Oncogene 7: 1867–1873.

    PubMed  CAS  Google Scholar 

  • Tsoulfas P, Soppet D, Escandon E, Tessarollo L, Rosenthal A, Nikolics K and Parada L (1993): The trkC locus encodes multiple neurogenic receptors that exhibit differential response to NT-3 in PC12 cells. Neuron 10: 975–990.

    Article  PubMed  CAS  Google Scholar 

  • Turner D and Cepko C (1987): A common progenitor for neurons and glia persists in rat retina late in development. Nature 328: 131–136.

    Article  PubMed  CAS  Google Scholar 

  • Turner D, Snyder E and Cepko C (1990): Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4: 833–845.

    Article  PubMed  CAS  Google Scholar 

  • Ullrich A and Schlessinger J (1990): Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212.

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela D, Maisonpierre P, Glass D, Rojas E, Nunez L, Kong Y, Gies D, Stitt T, Ip N and Yancopoulos G (1993): Alternative forms of rat TrkC with different functional capabilities. Neuron 10: 963–974.

    Article  PubMed  CAS  Google Scholar 

  • Vetter M, Martin Z, Parada L, Bishop J and Kaplan D (1991): Nerve growth factor rapidly stimulates tyrosine phosphorylation of phospholipase C-gamma 1 by a kinase activity associated with the product of the trk protooncogene. Proc Natl Acad Sci USA 88: 5650–5654.

    Article  PubMed  CAS  Google Scholar 

  • Walicke P (1988): Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J Neurosci 8: 2618–2627.

    PubMed  CAS  Google Scholar 

  • Walicke P, Cowan W, Ueno N, Baird A and Guillermin R (1986): Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc Natl Acad Sci USA 83: 817–821.

    Article  Google Scholar 

  • Wetmore C, Ernfors P, Persson H and Olson L (1990): Localization of brain-derived neurotrophic factor mRNA to neurons in the brain by in situ hybridization. Exp Neurol 109: 141–152.

    Article  PubMed  CAS  Google Scholar 

  • Wetts R and Fraser S (1988): Multipotent precursors can give rise to all major cell types of the frog retina. Science 239: 1142–1145.

    Article  PubMed  CAS  Google Scholar 

  • Witter M (1989): “Connectivity Of The Rat Hippocampus” (3 ed.). New York: Alan R. Liss, Inc.

    Google Scholar 

  • Wood K, Sarnecki C, Roberts T and Blenis J (1992): Ras mediates nerve growth factor receptor modulation of three signal transducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 68: 1041–1050.

    Article  PubMed  CAS  Google Scholar 

  • Yan Q and Johnson E (1988): An immunohistochemical study of the nerve growth factor receptor in developing rats. J Neurosci 8: 3481–3498.

    PubMed  CAS  Google Scholar 

  • Yankner B, Caceres A and Duffy L (1990a): Nerve growth factor potentiates the neurotoxicity of beta amyloid. Proc Natl Acad Sci USA 87: 9020–9023.

    Article  CAS  Google Scholar 

  • Yankner B, Duffy L and Kirschner D (1990b): Neurotrophic and neurotoxic effects of the amyloid beta protein are reversed by tachykinin neuropeptides. Science 250: 279–282.

    Article  CAS  Google Scholar 

  • Zafra F, Hengerer B, Leibrock J, Thoenen H and D, L. (1990). Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by nonNMDA glutamate receptors. EMBO J 9: 3545–3550.

    PubMed  CAS  Google Scholar 

  • Zimmer J and Gahwiler B (1984): Cellular and connective organization of slice cultures of the rat hippocampus and fascia dentata. J Comp Neurol 228: 432–446.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. LMB/NINDS, Building 36, Room 3D02, NIH, Bethesda, MD, 20892, USA

    Diana Collazo & Ron McKay

Authors
  1. Diana Collazo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ron McKay
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Saskatchewan, Saskatoon, Saskatchewan, Canada

    J. Ronald Doucette

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer Science+Business Media New York

About this chapter

Cite this chapter

Collazo, D., McKay, R. (1995). Neurotrophins and TRK Receptors in Hippocampal Development. In: Juurlink, B.H.J., Krone, P.H., Kulyk, W.M., Verge, V.M.K., Doucette, J.R. (eds) Neural Cell Specification. Altschul Symposia Series, vol 3. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1929-4_12

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-1929-4_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5790-2

  • Online ISBN: 978-1-4615-1929-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation