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Integrated axon-synapse unit in the central nervous system

  • A. Cestelli
  • G. Savettieri
  • I. Di Liegro
Part of the Topics in Anaesthesia and Critical Care book series (TIACC)

Abstract

One of the most daunting questions in developmental neurobiology concerns the mechanisms which allow cohorts of neurons to develop the intricate, yet stereotypic pattern of connections in the adult nervous system: it has been estimated that 1011 neurons of human brain establish a network of 1014 synaptic contacts. We must consider, however, that most neurons are generally grouped into classes with a characteristic pattern of connectivity and this mere fact allows the wiring of complex neural networks to be controlled by the reiteration and diversification of a relatively small number of prototypic connection patterns. On the other hand, it is a matter of fact that axon projection to the corresponding targets, which is a key element in the assembly of the nervous system, links the early inductive interactions that establish neuronal identity to the later steps of synapse formation. It is worth remembering that in the last decade it has been demonstrated that the exocytic trafficking system, which is the heart of the synaptic machinery, represents one of the most fascinating examples of conservation of a complex biological system throughout evolution, from yeast to vertebrates [1]. Neurons extend axons and dendrites through an outstanding variety of environments using a specialized structure which each of them has at its end, the growth cone [2, 3]. Growth cones detect and respond to information from their immediate environment by extending filopodia and lamellae that are endowed with a panoplia of receptors.

Keywords

Nerve Growth Factor Neurite Outgrowth Fibroblast Growth Factor Receptor Axonal Growth Neural Cell adheSIOn Molecule 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Ferro-Novick S, Jahn R (1994) The molecular machinery of secretion is conserved from yeast to neurons. Proc Natl Acad Sci 90: 2559–2563Google Scholar
  2. 2.
    Tessier-Lavigne M, Goodman CS (1996) The molecular mechanisms of axon guidance. Science 274: 1123–1133PubMedCrossRefGoogle Scholar
  3. 3.
    Stoeckli ET, Lendmesser LT (1998) Axon guidance at choice points. Curr Opin Neurobiol 8: 73–79PubMedCrossRefGoogle Scholar
  4. 4.
    Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454–1468PubMedGoogle Scholar
  5. 5.
    Bradke F, Dotti CG (1997) Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19: 1175–1186PubMedCrossRefGoogle Scholar
  6. 6.
    Higgins D, Burack M, Lein P, Banker G (1997) Mechanisms of neuronal polarity. Curr Opin Neurobiol 7: 599–604PubMedCrossRefGoogle Scholar
  7. 7.
    Eaton S, Simons K (1995) Apical, basal, and lateral cues for epithelial polarization. Cell 82: 5–8PubMedCrossRefGoogle Scholar
  8. 8.
    Ehlers MD, Mammen AL, Lau LF, Huganir RL (1996) Synaptic targeting of glutamate receptors. Curr Biol 8: 484–489Google Scholar
  9. 9.
    Tienan PJ, De Strooper B, Ikonen E, Simons M, Weidemann A, Czech C, Hartman T, Ida N, Multhaup G, Masters GL, Masters CL, van Leuven F, Beyreuther K, Dotti CG (1996) The 13-amyloid domain is essential for axonal sorting of amyloid precursor protein. EMBO J 15: 5218–5229Google Scholar
  10. 10.
    Jareb M, Banker G (1998) The polarized sorting of membrane proteins expressed in culture hippocampal neurons using viral vectors. Neuron 20: 855–867PubMedCrossRefGoogle Scholar
  11. 11.
    Lewin GR, Barde YA (1996) The physiology of neurotrophins. Annu Rev Neurosci 19: 289–317PubMedCrossRefGoogle Scholar
  12. 12.
    Cabelh RJ, Hohn A, Shatz CJ (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267: 1662–1666CrossRefGoogle Scholar
  13. 13.
    Cabelli RJ, Shelton DL, Segal R, Shatz CJ (1997) Blockade of endogenous ligands of TrkB inhibits formation of ocular dominance columns. Neuron 19: 63–75PubMedCrossRefGoogle Scholar
  14. 14.
    Brummendorf T, Rathjen FG (1995) Cell adhesion molecules 1: immunoglobulin superfamily. Protein Profile 2: 963–1108PubMedGoogle Scholar
  15. 15.
    Walsh FS, Doherty P (1997) Neural cell adhesion molecules of the immunoglobulin superfamily. Annu Rev Cell Biol 13: 425–456CrossRefGoogle Scholar
  16. 16.
    Pesheva P, Gennarini G, Goridis C, Schachner M (1993) The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1160/180. Neuron 10: 69–82PubMedCrossRefGoogle Scholar
  17. 17.
    Norenberg U, Hubert M, Brummendorf T, Tarnok A, Rathjen FG (1995) Characterization of functional domains of the tenascin-R (restrictin) polypeptide-cell attachment site, binding with F11, and enhancement of F11-mediated neurite outgrowth by tenascin-R. J Cell Biol 130: 473–484PubMedCrossRefGoogle Scholar
  18. 18.
    Wong EV, Kenwrick S, Willelms P, Lemmon V (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci 18: 168–172PubMedCrossRefGoogle Scholar
  19. 19.
    Cohen NR, Taylor JSH, Scott LB, Guillery RW, Soriano P, Furley AJW (1998) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule Ll Curr Biol 8 26–33Google Scholar
  20. 20.
    Walsh FS, Doherty P (1991) Structure and function of the gene for neural cell adhesion molecule Semin Neurosci 3: 271–284Google Scholar
  21. 21.
    Walsh FS, Doherty P (1997) Neural cell adhesion molecules of the immunoglobulin superfamily. Annu Rev Cell Dev Biol 13. 425–456PubMedCrossRefGoogle Scholar
  22. 22.
    Kiss JZ, Rougon G (1997) Cell biology of polysialic acid Curr. Opin Neurobiol 7: 640–646PubMedCrossRefGoogle Scholar
  23. 23.
    Doherty P, Walsh FS (1994) Signal transduction events underlying neunte outgrowth stimulated by cell adhesion molecules. Curr Opin Neurobiol 4: 49–55PubMedCrossRefGoogle Scholar
  24. 24.
    Doherty P, Walsh FS (1996) CAM-FGF receptor interactions: a model for axonal growth. Mol Cell Neurosci 8: 99–111CrossRefGoogle Scholar
  25. 25.
    Brittis PA, Silver J, Walsh FS, Doherty P (1996) FGF receptor function is required for the orderly projection of ganglion cell axons in the developing mammalian retina. Mol Cell Neurosci 8: 120–128CrossRefGoogle Scholar
  26. 26.
    Saffell JL, Williams EJ, Mason IJ, Walsh FS, Doherty P (1997) Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18: 232–242CrossRefGoogle Scholar
  27. 27.
    Eph Nomenclature Committee (1997) Unified nomenclature for Eph family receptors and their ligands. Cell 90: 403–404CrossRefGoogle Scholar
  28. 28.
    Holland SJ, Peles E, Pawson T, Schlessinger J (1998) Cell-contact-dependent signalling in axon growth and guidance: Eph receptor tyrosine kinases and receptor protein tyrosine phosphatase (3. Curr Opin Neurobiol 8: 117–127PubMedCrossRefGoogle Scholar
  29. 29.
    Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartimentalized during embryogenesis Neuron 17: 9–19Google Scholar
  30. 30.
    Kolodkm AL, Ginty DD (1997) Steering clear of semaphorms: neuropilins sound the retreat. Neuron 19: 1159–1162CrossRefGoogle Scholar
  31. 31.
    Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H (1997) Neurophilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19.995–1005Google Scholar
  32. 32.
    Carlson SS, Hockfield S (1996) Central nervous system. In: Comper WD (ed) Tissue Function. Extracellular matrix. Vol I. Harwood Academic, Amsterdam, pp 1–23Google Scholar
  33. 33.
    Small DH, San Mok S, Williamson TG, Nurcombe V (1996) Role of proteoglycans in neural development, regeneration, and the aging brain. J Neurochem 67: 889–899PubMedCrossRefGoogle Scholar
  34. 34.
    Cestelli A, Savettieri G, Salemi G, Di Liegro I (1992) Neuronal cell cultures: a tool for investigations in developmental neurobiology. Neurochem Res 17: 1163–1180PubMedCrossRefGoogle Scholar
  35. 35.
    Cohen J, Burne JF, McKinlay C, Winter J (1987) The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Dev Biol 122: 407–418PubMedCrossRefGoogle Scholar
  36. 36.
    Savettieri G, Mazzola GA, Rodriguez Sanchez MB, Caruso G, Di Liegro I, Cestelli A (1998) Modulation of synapsm I gene expression in rat cortical neurons by extracellular matrix. Cell Mol Neurobiol 18: 369–378PubMedCrossRefGoogle Scholar
  37. 37.
    Faissner A, Kruse J (1990) J 1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5: 627–637Google Scholar
  38. 38.
    Cook G, Tannahill D, Keynes R (1998) Axon guidance to and from choice points. Curr Op Neurobiol 8: 64–72PubMedCrossRefGoogle Scholar
  39. 39.
    Savettieri G, Cestelli A, Di Liegro I (1996) Biochemistry of neurotransmission: an update. In: Gullo A (ed) Anaesthesia, pain, intensive care and emergency medicine. Springer-Verlag, Berlin Heidelberg New York, pp 43–73Google Scholar
  40. 40.
    TolkoskyA (1997) Neurotrophic factors in action. Trends Neurosci 20: 1–3CrossRefGoogle Scholar
  41. 41.
    Schimmang T, Represa J (1997) Neurotrophins gain a hearing. Trends Neurosci 20: 100–102PubMedCrossRefGoogle Scholar
  42. 42.
    Marty S, da Penha Berzaghi M, Berninger B (1997) Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci 20: 198–202PubMedCrossRefGoogle Scholar
  43. 43.
    Bredesen DE, Rabizadeh S (1997) p75NTR and apoptosis: Trk-dependent and Trk-independent effects. Trends Neurosci 20: 287–290PubMedCrossRefGoogle Scholar
  44. 44.
    Carter BD, Lewin GR (1997) Neurotrophins lie or let die: does p75NTR decide? Neuron 18: 187–190PubMedCrossRefGoogle Scholar
  45. 45.
    Bergeron L, Yuan J (1998) Sealing one’s fate: control of cell death in neurons. Curr Opin Neurobiol 8: 55–63PubMedCrossRefGoogle Scholar
  46. 46.
    Chao MV (1994) The p75 neurotrophin receptor. J Neurobiol 25: 1373–1385PubMedCrossRefGoogle Scholar
  47. 47.
    Frade JM, Rodriguez-Tebar A, Barde YA (1996) Induction of cell death by endogenous nerve growth factor. Nature 383: 166–168PubMedCrossRefGoogle Scholar
  48. 48.
    Casaccia-Bonnefil P, Carter BD, Dobrovsky RT, Chao MV (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383: 716–719PubMedCrossRefGoogle Scholar
  49. 49.
    Dobrowsky RT, Werner MH, Castellino AM, Chao MV, Hannun YA (1994) Activation of the sphingomyelin cycle through the low affinity neurotrophin receptor. Science 265: 1596–1599PubMedCrossRefGoogle Scholar
  50. 50.
    Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhauser N, Bohm-Matthaei R, Baeuerle PA, Barde YA (1996) Selective activation of NF-kB by nerve growth factor through the neurotrophin receptor p75. Science 272: 542–545PubMedCrossRefGoogle Scholar
  51. 51.
    Phipott KL, McCarthy MJ, Kippel A, Rubin LL (1997) Activated phosphatidyl inositol 3-kinase promote surival of superior cervical neurons. J Cell Biol 139: 809–815CrossRefGoogle Scholar
  52. 52.
    O’Neill LAJ, Kaltschmidt C (1997) NK-kB: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20: 252–258PubMedCrossRefGoogle Scholar
  53. 53.
    Kaltschmidt C, Kaltschmidt B, Baeuerle PA (1993) Brain synapses contain inducible forms of the transcription factor NF-kB. Mech Dev 43: 135–147PubMedCrossRefGoogle Scholar
  54. 54.
    Meberg PJ, Kiney WR, Valcourt EG, Ruttenberg A (1996) Gene expression of the transcription factor NF-KB in hyppocampus: regulation by synaptic activity. Mol Brain Res 38: 179–190PubMedCrossRefGoogle Scholar
  55. 55.
    Blaustein JD, Lehman MN, Turcotte JC, Greene G (1992) Estrogen receptors in dendrites and axon terminals in the guinea pig hypothalamus. Endocrinology 131: 281–290PubMedCrossRefGoogle Scholar
  56. 56.
    Suter DM, Forscher P (1998) An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr Opin Neurobiol 8: 106–116PubMedCrossRefGoogle Scholar
  57. 57.
    Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ (1997) Actin dynamics in vivo. Curr Opin Cell Biol 9: 54–61PubMedCrossRefGoogle Scholar
  58. 58.
    Titus MA (1997) Unconventional myosins: new frontiers in actin-based motors. Trends Cell Biol 7: 119–123PubMedCrossRefGoogle Scholar
  59. 59.
    Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527–533PubMedCrossRefGoogle Scholar
  60. 60.
    Carlier MF (1998) Control of actin dynamics. Curr Opin Cell Biol 10: 45–51PubMedCrossRefGoogle Scholar
  61. 61.
    Ayscough KR (1998) In vivo functions of actin-binding proteins. Curr Opin Cell Biol 10: 102–111PubMedCrossRefGoogle Scholar
  62. 62.
    Welch MD, Iwamatsu A, Mitchison TJ (1997) Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes. Nature 385: 265–269PubMedCrossRefGoogle Scholar
  63. 63.
    Bray D (1997) The riddle of slow transport-an introduction. Trends Cell Biol 7: 379PubMedCrossRefGoogle Scholar
  64. 64.
    Baas PW, Brown A (1997) Slow axonal transport• the polymer transport model. Trends Cell Biol 7. 380–384PubMedCrossRefGoogle Scholar
  65. 65.
    Hirokawa N, Terada S, Funakoshi T, Takeda S (1997) Slow axonal transport: the subunit transport model Trends Cell Biol 7: 384–388Google Scholar
  66. 66.
    Heidemann SR (1996) Cytoplasmic mechanisms of axonal and dendritic growth in neurons Int Rev Cytol 165: 235–296Google Scholar
  67. 67.
    Delacourte A, Buée L (1997) Normal and pathological Tau proteins as factors for microtubule assembly Int Rev Cytol 171 167–224Google Scholar
  68. 68.
    Cunningham CC, Leclerc N, Flanagan LA, Janmey PA, Kosik KS (1997) Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J Cell Biol 136. 845–857PubMedCrossRefGoogle Scholar
  69. 69.
    Hirokawa N, Noda Y, Okada Y (1998) Kinesin and dynem superfamily proteins in organelle transport and cell division. Curr Opin Cell Biol 10: 60–73PubMedCrossRefGoogle Scholar
  70. 70.
    Hirokawa N (1998) Kinesin and dynem superfamily proteins and the mechanism of organelle transport. Science 279: 519–526PubMedCrossRefGoogle Scholar
  71. 71.
    Houseweart MK, Cleveland DW (1998) Intermediate filaments and their associated proteins: multiple dynamic personalities. Curr Opin Cell Biol 10: 93–101PubMedCrossRefGoogle Scholar
  72. 72.
    Yang Y, Dowling J, Yu QC, Kouklis P, Cleveland DW (1996) An essential cytoskeletal protein connecting actin microfilaments to intermediate filaments. Cell 86: 655–665PubMedCrossRefGoogle Scholar
  73. 73.
    Nixon RA (1998) The slow axonal transport of cytoskeletal proteins. Curr Opin Cell Biol 10: 87–92PubMedCrossRefGoogle Scholar
  74. 74.
    Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509–514PubMedCrossRefGoogle Scholar
  75. 75.
    Schlaepfer DD, Hunter T (1998) Integrin signalling and tyrosine phosphorylation: lust the FAKs? Trends Cell Biol 8: 151–157PubMedCrossRefGoogle Scholar
  76. 76.
    Howe A, Aplin AE, Alahari SK, Juliano RL (1998) Integren signaling and cell growth control. Curr Opin Cell Biol 10: 220–231PubMedCrossRefGoogle Scholar
  77. 77.
    Gebbink MF, Kranenburg O, Poland, M, van Horck FP, Houssa B, Moolenaar WH (1997) Identification of a novel, putative Rho-specific GDP/GTP exchange factor and a RhoA-binding protein• control of neuronal morphology. J Cell Biol 137. 1603–1613PubMedCrossRefGoogle Scholar
  78. 78.
    Bito H, Deisseroth K, Tsien RW (1997) Ca++-dependent regulation in neuronal gene expression Curr Opin Neurobiol 7: 419–429Google Scholar
  79. 79.
    Mikoshiba K (1997) The InsP3 receptor and intracellular Ca2+ signaling. Curr Opin Neurobiol 7: 339–345PubMedCrossRefGoogle Scholar
  80. 80.
    Holland SJ, Gale NW, Gish GD, Roth RA, Songyang Z, Cantley LC, Henkemeyer M, Yancopoulos GD, Pawson T (1997) Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells EMBO J 16: 3877–3888Google Scholar
  81. 81.
    Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20: 84–91PubMedCrossRefGoogle Scholar
  82. 82.
    Gallo G, Letourneau PC (1998) Axon guidance: GTPases help axons reach their targets Curr Bio18:R80–R82Google Scholar
  83. 83.
    Brosamle C (1998) The making, changing, and breaking of contacts. Trends Neurosci 21: 91–94PubMedCrossRefGoogle Scholar
  84. 84.
    Sheperd GM, Erulkar SD (1997) Centenary of the synapse: from Sherrington to the molecular biology of the synapse and beyond Trends Neurosci 20: 385–392Google Scholar
  85. 85.
    Changeux JP (1997) Letter to the editor. Trends Neuroses 7: 291–293Google Scholar
  86. 86.
    Purves D, White L, Riddle D (1997) Letter to the editor. Trends Neuroses 7: 293Google Scholar
  87. 87.
    Davis GW, Goodman CS (1998) Genetic analysis of synaptic development and plasticity: homeostatic regulation of synaptic efficacy. Curr Opin Neurobiol 8. 149–156PubMedCrossRefGoogle Scholar

Copyright information

© Springer Verlag Italia, Milano 1999

Authors and Affiliations

  • A. Cestelli
  • G. Savettieri
  • I. Di Liegro

There are no affiliations available

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