Sorting and Intracellular Transport of RNA in Neurons: Regulation of Gene Expression at Synaptic Sites

  • Oswald Steward
  • Robin Kleiman
  • Gary Banker
Part of the Basic and Clinical Aspects of Neuroscience book series (BASIC, volume 6)

Abstract

It has been recognized since the time of Cajal that different parts of the neuron are specialized for different functions; indeed, this is the basis for what Cajal called the “dynamic polarization of the neuron.” Axons are specialized for transmitting information over great distances, dendrites and cell bodies for receiving and integrating inputs from other cells, and synapses for communicating information from one neuron to the next. Each of these functional attributes depends upon two features: (1) the “molecular anatomy” of the neuron, which includes the composition and spatial distribution of receptors, channels, etc. in the neuronal plasma membrane and the intracellular distribution of organelles, second messenger systems, and enzyme systems; and (2) neuronal microstructure, i. e., the shape and spatial configuration of axons, dendrites, and the synaptic connections between them.

Keywords

Codon Neurol NMDA Fibril Acetylcholine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Autilio LA, Appel SH, Pettis P and Gambetti P (1968) Biochemical studies of synapses in vitro. 1. Protein synthesis. Biochem 7: 2615–2622CrossRefGoogle Scholar
  2. 2.
    Bruckenstein DA, Lein PJ, Higgins D, Fremeau RT (1990) Distinct spatial localization of specific mRNAs in cultured sympathetic neu-rons. Neuron 5: 809–819PubMedCrossRefGoogle Scholar
  3. 3.
    Burgin KE, Washam MN, Rickling S, Westgate SA, Mobley WC, Kelly PT (1990) In situ hybridization histochemistry of CA++/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 10: 1788–1798PubMedGoogle Scholar
  4. 4.
    Changeux JP et al. (1990) Compartmentalization of acetylcholine receptor gene expression during development of the neuromuscular junction. Cold Spring Harbor Symp Quant Biol 55: 381–396PubMedGoogle Scholar
  5. 5.
    Chicurel ME, Terrian DM, Potter H (1993) mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J. Neurosci 13: 4054–4064Google Scholar
  6. 6.
    Davis L, Banker GA, Steward O (1987) Selective dendritic transport of RNA in hippocampal neurons in culture. Nature 330: 447–479CrossRefGoogle Scholar
  7. 7.
    Davis L, Burger B, Banker G, Steward O (1990) Dendritic transport: quantitative analysis of the time course of somatodendritic transport of recently synthesized RNA. J Neurosci 10: 3056–3058PubMedGoogle Scholar
  8. 8.
    Deadwyler SA, Dunwiddie T, Lynch G (1987) A critical level of protein synthesis is required for long-term potentiation. Synapse 1: 90–95PubMedCrossRefGoogle Scholar
  9. 9.
    DeChiara TM, Brosius J (1987) Neural BC1 RNA: cDNA clones reveal nonrepetitive sequence content. Proc Natl Acad Sci USA 84: 2624–2628PubMedCrossRefGoogle Scholar
  10. 10.
    Feig S, Lipton P (1993) Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. J. Neurosci 13: 1010–1021PubMedGoogle Scholar
  11. 11.
    Fifkova E, Delay RJ (1982) Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 95: 345–350PubMedCrossRefGoogle Scholar
  12. 12.
    Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452: 57–65PubMedCrossRefGoogle Scholar
  13. 13.
    Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M (1986) Structure and segmentation gene paired and the drosophila PRD gene set as part of a gene network. Cell 47: 735–746PubMedCrossRefGoogle Scholar
  14. 14.
    Gallo V, Upson LM, Hayes WP, Vyklicky LJ, Winters CA, Buonanno A (1992) Molecular cloning and developmental analysis of a new glutamate receptor subunit isoform in cerebellum. J Neurosci 12: 1010–1023PubMedGoogle Scholar
  15. 15.
    Gambetti P, Autilio-Gambetti LA, Gonatas NK, Shafer B (1972) Protein synthesis in synaptosomal fractions: ultrastructural radioautographic study. J Cell Biol 52: 526–535PubMedCrossRefGoogle Scholar
  16. 16.
    Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336: 674–677PubMedCrossRefGoogle Scholar
  17. 17.
    Giuditta A, Hunt T, Santella L (1986) Messenger RNA in squid axoplasm. Neurochem Int 8: 435–442PubMedCrossRefGoogle Scholar
  18. 18.
    Higgins GA, Lewis DA, Bahmanyar S, Goldgaber D, Gajdusek DC, Young WG, Morrison JH, Wilson MC (1988) Differential regulation of amyloid β-protein mRNA expression within hippocampal neuronal subpopulations in Alzheimer disease. Proc Natl Acad Sci USA 85: 1297–1301PubMedCrossRefGoogle Scholar
  19. 19.
    Jeffery WR (1985) Specification of cell fate by cytoplasmic determinants in ascidian embryos. Cell 41: 11–12PubMedCrossRefGoogle Scholar
  20. 20.
    Kennedy MB, Bennett MK, Bulleit RF, Erondu NE, Jennings VR, Miller SG, Molloy SS, Patton BL, Sehender LJ (1990) Structure and regulation of type II calcium/calmodulin-dependent protein kinase in central nervous system neurons. Cold Spring Harbor Symp Quant Biol: 101–110Google Scholar
  21. 21.
    Kislauskis EH, Singer RH (1991) Characterization of sequences responsible for peripheral localization of β-actin mRNA. J Cell Biol 115: 158AGoogle Scholar
  22. 22.
    Klausner RD, Harford JB (1989) Cis-trans models for post-transcriptional gene regulation. Science 246: 870 - 872PubMedCrossRefGoogle Scholar
  23. 23.
    Kleiman R, Banker G, Steward O (1990) Differential subcellular localization of particular mRNAs in hippocampal neurons in culture. Neuron 5: 821–830PubMedCrossRefGoogle Scholar
  24. 24.
    Kleiman R, Banker GA, Steward O (in press) Subcellular distribution of rRNA and Poly-A RNA in hippocampal neurons in culture. Mol Brain ResGoogle Scholar
  25. 25.
    Kleiman R, Banker GA, Steward O (in press) Development of sub-cellular mRNA compartmentation in hippocampal neurons in culture. J. NeurosciGoogle Scholar
  26. 26.
    Kobayashi S, Goto S, Anzai K (1991) Brain-specific small RNA transcript of the identifier sequences is present as a 10 S ribonucleoprotein particie. J Biol Chem 266 (8): 4726–41730PubMedGoogle Scholar
  27. 27.
    Koenig E, Adams P (1982) Local protein synthesizing activity in ax- onal fields regenerating in vitro. J Neurochem 39: 386–400PubMedCrossRefGoogle Scholar
  28. 28.
    Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13: 39–42PubMedCrossRefGoogle Scholar
  29. 29.
    Lasek RJ, Dabrowsky JC, Nordlander R (1973) Analysis of axoplasmic RNA from invertebrate giant axons. Nature 244: 162–165CrossRefGoogle Scholar
  30. 30.
    Lawrence JB, Singer RH (1986) Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45: 407–415PubMedCrossRefGoogle Scholar
  31. 31.
    Lehmann R, Nusslein-Volhard C (1991) The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112: 679 - 693PubMedGoogle Scholar
  32. 32.
    Lewis DA, Higgins GA, Young WG, Goldgaber D, Gajdusek DC, Wilson MC, Morrison JH (1988) Distribution of precursor amyloid β-protein messenger RNA in human cerebral cortex: Relationship to neurofibrillary tangles and neuritic plaques. Proc Natl Acad Sci USA 85: 1691–1695PubMedCrossRefGoogle Scholar
  33. 33.
    MacDonald PM (1990) Bicoid MRNA localization signal: phylogenetic conservation of function and RNA secondary structure. Development 110: 161–171PubMedGoogle Scholar
  34. 34.
    MacDonald PM, Struhl G (1986) A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324: 537–545PubMedCrossRefGoogle Scholar
  35. 35.
    MacDonald PM, Struhl G (1988) Cis-acting sequences responsible for anterior localization of bicold mRNA in Drosophila embryos. Nature 336: 595–598PubMedCrossRefGoogle Scholar
  36. 36.
    Martin R, Fritz W, Giuditta A (1989) Visualization of polyribosomes in the postsynaptic area of the squid giant synapse by electron spectroscopic imaging. J Neurocytol 18: 11–18PubMedCrossRefGoogle Scholar
  37. 37.
    Matus A, Bernhardt R, Hugh-Jones T (1981) HMW proteins are preferentially associated with dendritic microtubules in brain. Proc Natl Acad Sci USA 78: 3010–3014PubMedCrossRefGoogle Scholar
  38. 38.
    Meiton DA (1991) Pattern formation during animal development. Science 252: 224–241Google Scholar
  39. 39.
    Merlie JP, Sanes JA (1985) Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibers. Nature 317: 66–68PubMedCrossRefGoogle Scholar
  40. 40.
    Molloy SS, Kennedy MB (1991) Autophosphorylation of type II Ca2+/calmodulin-dependent protein kinase in cultures of postnatal rat hippocampal slices. Proc Natl Acad Sci USA 88: 4756–4760PubMedCrossRefGoogle Scholar
  41. 41.
    Mowry K, Melton DA (1991) Localization of mRNA in frog oocytes and eggs. J Cell Biol 115:123 AGoogle Scholar
  42. 42.
    Murphy D, Levy A, Lightman S, Carter D (1989) Vasopressin RNA in the neural lobe of the rat pituitary: dramatic accumulation in response to salt loading. Proc Natl Acad Sci USA 86: 9002–9005PubMedCrossRefGoogle Scholar
  43. 43.
    Otani S, Marshall CJ, Tate WP, Goddard GV, Abraham WC (1989) Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediate post-tetanization. Neuroscience 28: 519–526PubMedCrossRefGoogle Scholar
  44. 44.
    Palacios-Pru EL, Palacios L, Mendoza RV (1981) Synaptogenetic mechanisms during chick cerebellar cortex development. J Submi- crosc Cytol Pathol 13: 145–167Google Scholar
  45. 45.
    Phillips LL, Nostrandt SJ, Chikaraishi DM, Steward O (1987) Increases in ribosomal RNA within the denervated neuropil of the dentate gyrus during reinnervation: evaluation by in situ hybridization using DNA probes complementary to ribosomal RNA. Mol Brain Res 2: 251–261CrossRefGoogle Scholar
  46. 46.
    Rao A, Steward O (1991) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized Within synaptosomes. J Neurosci 11: 2881–2895PubMedGoogle Scholar
  47. 47.
    Rao A, Steward O (1993) Evaluation of RNAs present in synaptodendrosomes: dendritic, glial and neuronal cell body contribution. J Neurochem 835–844Google Scholar
  48. 48.
    Sarthy PV, Fu M, Huang J (1989) Subcellular localization of an intermediate filament protein and its mRNA in glial cells. Mol Cell Biol 9: 4556–4559PubMedGoogle Scholar
  49. 49.
    Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992) Deficient hippocampal long-term potentiation in alpha-calcium-caimodulin kinase II mutant mice. Science 257: 201–206PubMedCrossRefGoogle Scholar
  50. 50.
    Stanton PK, Sarvey JM (1984) Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J Neurosci 4: 3080–3088PubMedGoogle Scholar
  51. 51.
    Steward O (1983) Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat. J Neurosci 3: 177–188PubMedGoogle Scholar
  52. 52.
    Steward O, Banker GA (1992) Getting the message from the gene to the synapse: sorting and intracellular transport of RNA in neu-rons. Trends Neurosci 15: 180–186PubMedCrossRefGoogle Scholar
  53. 53.
    Steward O, Falk PM (1986) Protein synthetic machinery at post-synaptic sites during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses. J Neurosci 6: 412–423PubMedGoogle Scholar
  54. 54.
    Steward O, Levy WB (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2: 284–291PubMedGoogle Scholar
  55. 55.
    Steward O, Reeves TM (1988) Protein synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J Neurosci 8: 176–184PubMedGoogle Scholar
  56. 56.
    Steward O, Ribak CE (1986) Polyribosomes associated with synaptic sites on axon initial segments: localization of protein synthetic machinery at inhibitory synapses. J Neurosci 6: 3079–3085PubMedGoogle Scholar
  57. 57.
    Strong MJ, Svedmyr A, Gajdusek DC, Garruto RM (1990) The temporal expression of amyloid precursor protein mRNA in vitro in dissociated hippocampal neuron cultures. Exp Neurol 109: 171–179PubMedCrossRefGoogle Scholar
  58. 58.
    Struhl G (1989) Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338: 741–744PubMedCrossRefGoogle Scholar
  59. 59.
    Sutcliffe JG, Milner RJ, Gottesfeld JM, Reynolds W (1984) Control of neuronal gene expression. Science 225: 1308–1315PubMedCrossRefGoogle Scholar
  60. 60.
    Tiedge H, Chen W, Brosius J (1993) Primary structure, neural-specific expression, and dendritic location of human BC200 RNA. J Neurosci 13: 2382–2390PubMedGoogle Scholar
  61. 61.
    Tiedge H, Fremeau RT Jr, Weinstock PH, Arancio O, Brosius J (1991) Dendritic location of neural BC1 RNA. Proc Natl Acad Sci USA 88: 2093–2097PubMedCrossRefGoogle Scholar
  62. 62.
    Torre ER, Steward O (1992) Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies. J Neurosci 12: 762–772PubMedGoogle Scholar
  63. 63.
    Trapp BD, Moench T, Pulley M, Barbosa E, Tennekoon G, Griffin J (1987) Spatial segregation of mRNA encoding myelin-specific proteins. Proc Natl Acad Sci USA 84: 7773–7777PubMedCrossRefGoogle Scholar
  64. 64.
    Tucker RP, Garner CC, Matus A (1989) In situ localization of micro- tubule-associated protein mRNA in the developing and adult rat brain. Neuron 2: 1245–1256PubMedCrossRefGoogle Scholar
  65. 65.
    Weiler IJ, Greenough WT (1991) Potassium ion stimulation triggers protein translation in ynaptoneuronsomal polyribosomes. Molec Cell Neurosci 2: 305–314PubMedCrossRefGoogle Scholar
  66. 66.
    Yisraell JK, Melton DA (1988) The maternal mRNA Vgl is correctly localized following injection into Xenopus oocytes. Nature 336: 592–595CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • Oswald Steward
    • 1
    • 2
  • Robin Kleiman
    • 1
    • 2
  • Gary Banker
    • 1
    • 2
  1. 1.Department of NeuroscienceUniversity of Virginia Health Sciences CenterCharlottesvilleUSA
  2. 2.Department of NeurosurgeryUniversity of Virginia Health Sciences CenterCharlottesvilleUSA

Personalised recommendations