Translational Machinery in Dendrites of Hippocampal Neurons in Culture

In neurons, several mRNAs are selectively delivered to dendritic domains where they are presumably translated by local protein synthetic machinery. Although electron microscopy has identified polyribosomes in dendrites, in particular in postsynaptic dendritic compartments, the functional composition of the local protein synthetic apparatus and the scope of its translational capacity have not been analyzed. To ascertain the translational competence of dendrites, we have probed hippocampal neurons in primary culture for various integral and associated factors of the translational apparatus. We report here that dendrites of such neurons are equipped with a spectrum of translational machinery components, including ribosomes, tRNAs, initiation and elongation factors, and elements of the cotranslational signal recognition mechanism. These components are differentially and nonuniformly distributed in dendritic arbors. Their dendritic location illustrates the soma-independent potential of dendrites to synthesize selected proteins in local domains.

[1]  J. Brosius,et al.  Identification and characterization of BC1 RNP particles. , 1996, DNA and cell biology.

[2]  S. Fuller,et al.  The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons. , 1995, Molecular biology of the cell.

[3]  U. Frey,et al.  Somatodendritic expression of an immediate early gene is regulated by synaptic activity. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Daniel St Johnston,et al.  The intracellular localization of messenger RNAs , 1995, Cell.

[5]  O. Steward Targeting of mRNAs to subsynaptic microdomains in dendrites , 1995, Current Opinion in Neurobiology.

[6]  Carol A Barnes,et al.  Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites , 1995, Neuron.

[7]  J. Eberwine,et al.  On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[8]  O. Steward,et al.  Dendrites as compartments for macromolecular synthesis. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. De Camilli,et al.  Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  G. Banting,et al.  Polarized Distribution of the Trans‐Golgi Network Marker TGN38 During the In Vitro Development of Neocortical Neurons: Effects of Nocodazole and Brefeldin A , 1994, The European journal of neuroscience.

[11]  O. Steward,et al.  Development of subcellular mRNA compartmentation in hippocampal neurons in culture , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  M P Deutscher,et al.  Supramolecular organization of the mammalian translation system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  O. Steward,et al.  Subcellular distribution of rRNA and poly(A) RNA in hippocampal neurons in culture. , 1993, Brain research. Molecular brain research.

[14]  R. Vale,et al.  RNA on the move: the mRNA localization pathway [published erratum appears in J Cell Biol 1993 Dec;123(6 Pt 1):1625] , 1993, The Journal of cell biology.

[15]  D. Terrian,et al.  mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  O. Steward,et al.  Evaluation of RNAs Present in Synaptodendrosomes: Dendritic, Glial, and Neuronal Cell Body Contribution , 1993, Journal of neurochemistry.

[17]  I. Weiler,et al.  Metabotropic glutamate receptors trigger postsynaptic protein synthesis. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Huganir,et al.  The distribution of glutamate receptors in cultured rat hippocampal neurons: Postsynaptic clustering of AMPA selective subunits , 1993, Neuron.

[19]  R. Rhoads Regulation of eukaryotic protein synthesis by initiation factors. , 1993, The Journal of biological chemistry.

[20]  R. Singer,et al.  Determinants of mRNA localization. , 1992, Current opinion in cell biology.

[21]  K M Harris,et al.  Three‐dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus , 1992, The Journal of comparative neurology.

[22]  O. Steward,et al.  Getting the message from the gene to the synapse: sorting and intracellular transport of RNA in neurons , 1992, Trends in Neurosciences.

[23]  O. Steward,et al.  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 , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M. Deutscher,et al.  Channeling of aminoacyl-tRNA for protein synthesis in vivo. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. De Camilli,et al.  The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Brosius,et al.  Dendritic location of neural BC1 RNA. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Kobayashi,et al.  Brain-specific small RNA transcript of the identifier sequences is present as a 10 S ribonucleoprotein particle. , 1991, The Journal of biological chemistry.

[28]  H. Tiedge The use of UV light as a cross-linking agent for cells and tissue sections in in situ hybridization. , 1991, DNA and cell biology.

[29]  S. Palay,et al.  The fine structure of the nervous system , 1991 .

[30]  T. Rapoport,et al.  The signal sequence receptor has a second subunit and is part of a translocation complex in the endoplasmic reticulum as probed by bifunctional reagents , 1990, The Journal of cell biology.

[31]  R. Fremeau,et al.  Distinct spatial localization of specific mRNAs in cultured sympathetic neurons , 1990, Neuron.

[32]  O. Steward,et al.  Differential subcellular localization of particular mRNAs in hippocampal neurons in culture , 1990, Neuron.

[33]  M. Waxham,et al.  In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  C. Godfraind,et al.  In vivo analysis of glial cell phenotypes during a viral demyelinating disease in mice , 1989, The Journal of cell biology.

[35]  A. Matus,et al.  Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites , 1988, Nature.

[36]  G. Banker,et al.  Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones , 1988, Nature.

[37]  M. Deutscher,et al.  A role for lipids in the functional and structural properties of the rat liver aminoacyl-tRNA synthetase complex. , 1988, The Journal of biological chemistry.

[38]  G. Banker,et al.  The establishment of polarity by hippocampal neurons in culture , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  H. Bielka,et al.  Shape and location of eukaryotic initiation factor eIF-2 on the 40S ribosomal subunit of rat liver. Immunoelectron-microscopic and hydrodynamic investigations. , 1988, European journal of biochemistry.

[40]  O. Steward,et al.  Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  A. Nairn,et al.  Identification of the major Mr 100,000 substrate for calmodulin-dependent protein kinase III in mammalian cells as elongation factor-2. , 1987, The Journal of biological chemistry.

[42]  P. De Camilli,et al.  Heterogeneous distribution of the cAMP receptor protein RII in the nervous system: evidence for its intracellular accumulation on microtubules, microtubule-organizing centers, and in the area of the Golgi complex , 1986, The Journal of cell biology.

[43]  G. Banker,et al.  Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  O. Steward,et al.  Protein-synthetic machinery at postsynaptic sites during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  A. Nairn,et al.  Identification of calmodulin-dependent protein kinase III and its major Mr 100,000 substrate in mammalian tissues. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[46]  K. Elkon,et al.  Lupus autoantibodies target ribosomal P proteins , 1985, The Journal of experimental medicine.

[47]  P. Greengard,et al.  A 38,000-dalton membrane protein (p38) present in synaptic vesicles. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Ullu,et al.  Alu sequences are processed 7SL RNA genes , 1984, Nature.

[49]  M. Deutscher The eucaryotic aminoacyl-tRNA synthetase complex: suggestions for its structure and function , 1984, The Journal of cell biology.

[50]  G. Banker,et al.  An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  G. Banker,et al.  An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. Synaptic relationships , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  G. Blobel,et al.  Subcellular distribution of signal recognition particle and 7SL-RNA determined with polypeptide-specific antibodies and complementary DNA probe , 1983, The Journal of cell biology.

[53]  O. Steward Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Peter Walter,et al.  Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum , 1982, Nature.

[55]  E. Ullu,et al.  Human 7SL RNA consists of a 140 nucleotide middle-repetitive sequence inserted in an Alu sequence , 1982, Cell.

[56]  W. Levy,et al.  Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  E. Palacios-Prü,et al.  Synaptogenetic mechanisms during chick cerebellar cortex development. , 1981, Journal of submicroscopic cytology.

[58]  V. Tennyson The Fine Structure of the Nervous System. , 1970 .

[59]  P. Walter,et al.  Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. , 1994, Annual review of cell biology.

[60]  J. van Minnen RNA in the axonal domain: a new dimension in neuronal functioning? , 1994, The Histochemical journal.

[61]  A Miyawaki,et al.  Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. , 1993, Receptors & channels.

[62]  J. Hershey,et al.  Translational control in mammalian cells. , 1991, Annual review of biochemistry.

[63]  T. Rapoport,et al.  A signal sequence receptor in the endoplasmic reticulum membrane , 1987, Nature.

[64]  E. Gray The Fine Structure of the Nervous System , 1971 .