Skip to main content

Protein Synthesis in Nerve Terminals and the Glia–Neuron Unit

  • Chapter
  • First Online:
Cell Biology of the Axon

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 48))

Abstract

The progressive philogenetic lengthening of axonal processes and the increase in complexity of terminal axonal arborizations markedly augmented the demands of the neuronal cytoplasmic mass on somatic gene expression. It is proposed that in an adaptive response to this challenge, novel gene expression functions developed in the axon compartment, consisting of axonal and presynaptic translation systems that rely on the delivery of transcripts synthesized in adjacent glial cells. Such intercellular mode of gene expression would allow more rapid plastic changes to occur in spatially restricted neuronal domains, down to the size of individual synapses. The cell body contribution to local gene expression in well-differentiated neurons remains to be defined. The history of this concept and the experimental evidence supporting its validity are critically discussed in this article. The merit of this perspective lies with the recognition that plasticity events represent a major occurrence in the brain, and that they largely occur at synaptic sites, including presynaptic endings.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover 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

Abbreviations

CAP:

Chloramphenicol

CXM:

Cycloheximide

EB:

Ethidium bromide

EM:

Electron microscopy

ESI:

Electron spectroscopic imaging

MW:

Molecular weight

NF:

Neurofilament

RNA bases:

A adenine, C cytosine, G guanine, U uracil

RNP:

Ribonucleoprotein particle

TH:

Tyrosine hydroxylase

References

  • Alvarez J, Giuditta A, Koenig E (2000) Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog Neurobiol 62:1–62

    PubMed  CAS  Google Scholar 

  • Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB (2008) Micro RNA-338 regulates local cytochrome oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J Neurosci 19:12581–12590

    Google Scholar 

  • Auld DS, Robitaille R (2003) Glial cells and neurotransmission: an inclusive view of synaptic function. Neuron 40:389–400

    PubMed  CAS  Google Scholar 

  • Austin L, Morgan IG (1967) Incorporation of 14C-labelled leucine into synaptosomes from rat cerebral cortex in vitro. J Neurochem 14:377–387

    PubMed  CAS  Google Scholar 

  • Autilio-Gambetti L, Gambetti P, Shafer B (1973) RNA and axonal flow. Biochemical and autoradiographic study in the rabbit optic system. Brain Res 53:387–398

    PubMed  CAS  Google Scholar 

  • Bacaj T, Tevlin M, Lu Y, Shaham S (2008) Glia are essential for sensory organ function in C. elegans. Science 322:744–747

    PubMed  CAS  Google Scholar 

  • Bains JS, Oliet SH (2007) Glia: they make your memories stick! Trends Neurosci 30:417–424

    PubMed  CAS  Google Scholar 

  • Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A, Izquierdo I, Medina JH (2008) BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci USA 105:2711–2716

    PubMed  CAS  Google Scholar 

  • Benech C, Sotelo JR Jr, Menendez J, Correa-Luna R (1982) Autoradiographic study of RNA and protein synthesis in sectioned peripheral nerves. Exp Neurol 76:72–82

    PubMed  CAS  Google Scholar 

  • Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7:613–620

    PubMed  CAS  Google Scholar 

  • Bittner GD (1991) Long-term survival of anucleate axons and its implications for nerve regeneration. Trends Neurosci 14:188–193

    PubMed  CAS  Google Scholar 

  • Brown MC, Perry VH, Hunt SP, Lapper SR (1994) Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration. Eur J Neurosci 6:420–428

    PubMed  CAS  Google Scholar 

  • Bunge RP (1993) Expanding roles for the Schwann cell: ensheathment, myelination, trophism and regeneration. Curr Opin Neurobiol 3:805–809

    PubMed  CAS  Google Scholar 

  • Cambray S, Pedraza N, Rafel M, Garí E, Aldea M, Gallego C (2009) Protein kinase KIS localizes to RNA granules and enhances local translation. Mol Cell Biol 29:726–735

    PubMed  CAS  Google Scholar 

  • Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237

    PubMed  CAS  Google Scholar 

  • Chihara T, Luginbuhl D, Luo L (2007) Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat Neurosci 10:828–837

    PubMed  CAS  Google Scholar 

  • Chun JT, Gioio AE, Crispino M, Giuditta A, Kaplan BB (1995) Characterization of squid enolase mRNA: sequence analysis, tissue distribution, and axonal localization. Neurochem Res 20:923–930

    PubMed  CAS  Google Scholar 

  • Chun JT, Gioio AE, Crispino M, Giuditta A, Kaplan BB (1996) Differential compartmentalization of mRNAs in squid giant axon. J Neurochem 97:1806–1812

    Google Scholar 

  • Chun JT, Gioio AE, Crispino M, Eyman M, Giuditta A, Kaplan BB (1997) Molecular cloning and characterization of a novel mRNA present in the squid giant axon. J Neurosci Res 49:144–153

    PubMed  CAS  Google Scholar 

  • Cohen AI (1973) An ultrastructural analysis of the photoreceptors of the squid and their synaptic connections. III. Photoreceptor terminations in the optic lobe. J Comp Neurol 147:399–426

    PubMed  CAS  Google Scholar 

  • Cotman CW, Taylor DA (1971) Autoradiographic analysis of protein synthesis in synaptosomal fractions. Brain Res 29:366–372

    Google Scholar 

  • Court F, Alvarez J (2005) Local regulation of the axonal phenotype, a case of merotropism. Biol Res 38:365–374

    PubMed  Google Scholar 

  • Court FA, Hendriks WT, Macgillavry HD, Alvarez J, van Minnen J (2008) Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J Neurosci 28:11024–11029

    PubMed  CAS  Google Scholar 

  • Crispino M, Capano CP, Kaplan BB, Giuditta A (1993a) Neurofilament proteins are synthesized in nerve endings from squid brain. J Neurochem 61:1144–1146

    CAS  Google Scholar 

  • Crispino M, Castigli E, Perrone Capano C, Martin R, Menichini E, Kaplan BB, Giuditta A (1993b) Protein synthesis in a synaptosomal fraction from squid brain. Mol Cell Neurosci 4:366–374

    CAS  Google Scholar 

  • Crispino M, Kaplan BB, Martin R, Alvarez J, Chun JT, Benech JC, Giuditta A (1997) Active polysomes are present in the large presynaptic endings of the synaptosomal fraction from squid brain. J Neurosci 17:7694–7702

    PubMed  CAS  Google Scholar 

  • Cupello A, Hydén H (1982) Labeling of poly(A)-associated RNA in synaptosomes and the other subcellular fractions of rat cerebral cortex in basal conditions and during training. J Neurosci Res 8:575–579

    PubMed  CAS  Google Scholar 

  • Cutillo V, Montagnese P, Gremo F, Casola L, Giuditta A (1983) Origin of axoplasmic RNA in the squid giant fibre. Neurochem Res 8:1621–1634

    PubMed  CAS  Google Scholar 

  • DeLarco J, Nakagawa S, Abramowitz A, Bromwell K, Guroff G (1975) Polyadenylic acid-containing RNA from rat brain synaptosomes. J Neurochem 25:131–137

    PubMed  CAS  Google Scholar 

  • Dirks RW, van Dorp AGM, van Minnen J, Fransen JAM, van der Ploeg M, Rapp AK (1993) Ultrastructural evidence for the axonal localization of caudodorsal cell hormone mRNA in the central nervous system of the mollusk Lymnea stagnalis. Microsc Res Techn 25:12–18

    CAS  Google Scholar 

  • Edström A (1964) Effect of spinal cord transection on the base composition and content of RNA in the Mauthner nerve fibre of the goldfish. J Neurochem 11:557–559

    Google Scholar 

  • Edström A (1966) Amino acid incorporation in isolated Mauthner nerve fibre components. J Neurochem 13:315–321

    Google Scholar 

  • Edström A (1967) Inhibition of protein synthesis in Mauthner nerve fibre components by actinomycin-D. J Neurochem 14:239–243

    PubMed  Google Scholar 

  • Edström A, Edström JE, Hökfelt T (1969) Sedimentation analysis of ribonucleic acid extracted from isolated Mauthner nerve fibre components. J Neurochem 16:53–66

    PubMed  Google Scholar 

  • Edström JE, Eichner D, Edström A (1962) The ribonucleic acid of axons and myelin sheaths from Mauthner neurons. Biochim Biophys Acta 61:178–184

    PubMed  Google Scholar 

  • Edström JE, Grampp W (1965) Nervous activity and metabolism of ribonucleic acids in the crustacean stretch receptor neuron. J Neurochem 12:735–741

    PubMed  Google Scholar 

  • England JM, Attardi G (1976) Analysis of RNA synthesized by an isolated rat brain synaptosomal fraction. J Neurochem 27:895–904

    Google Scholar 

  • Eyman M, Crispino M, Kaplan BB, Giuditta A (2003) Squid photoreceptor terminals synthesize calexcitin, a learning related protein. Neurosci Lett 347:21–24

    PubMed  CAS  Google Scholar 

  • Eyman M, Cefaliello C, Ferrara E, De Stefano R, Scotto Lavina Z, Crispino M, Squillace A, van Minnen J, Kaplan BB, Giuditta A (2007a) Local synthesis of RNA in axons and nerve terminals. Eur J Neurosci 25:341–350

    Google Scholar 

  • Eyman M, Ferrara E, Cefaliello C, Mandile P, Crispino M, Giuditta A (2007b) Synaptosomal protein synthesis from rat brain is selectively modulated by learning. Brain Res 1132:148–157

    CAS  Google Scholar 

  • Fellin T (2009) Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem 108:533–544

    PubMed  CAS  Google Scholar 

  • Fiore R, Siegel G, Schratt G (2008) MicroRNA function in neuronal development, plasticity and disease. Biochim Biophys Acta 1779:471–478

    PubMed  CAS  Google Scholar 

  • Fischer S, Litvak S (1967) The incorporation of micro injected 14C-aminoacids into TCA insoluble fractions of the giant axon of the squid. J Cell Physiol 70:69–74

    PubMed  CAS  Google Scholar 

  • Fischer S, Gariglio P, Tarifeno E (1969) Incorporation of H3-uridine and the isolation and the characterization of RNA from squid axon. J Cell Physiol 74:155–162 Pfeiffer BE, Huber

    PubMed  CAS  Google Scholar 

  • Flavell SW, Greenberg ME (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31:563–590

    PubMed  CAS  Google Scholar 

  • Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536

    PubMed  CAS  Google Scholar 

  • Gafurov B, Urazaev AK, Grossfeld RM, Lieberman EM (2001) N-acetylaspartylglutamate (NAAG) is the probable mediator of axon-to-glia signaling in the crayfish medial giant nerve fiber. Neuroscience 106:227–235

    PubMed  CAS  Google Scholar 

  • Gainer H (1978) Intercellular transfer of proteins from glial cells to axons. Trends Neurosci 1:93–96

    Google Scholar 

  • Gambetti P, Autilio-Gambetti LA, Gonatas NK, Shafer B (1972) Protein synthesis in synaptosomal fractions. Ultrastructural radioautographic study. J Cell Biol 52:526–535

    PubMed  CAS  Google Scholar 

  • Gioio AE, Chun JT, Crispino M, Perrone Capano C, Giuditta A, Kaplan BB (1994) Kinesin mRNA is present in the squid giant axon. J Neurochem 63:13–18

    PubMed  CAS  Google Scholar 

  • Gioio AE, Eyman M, Zhang H, Lavina ZS, Giuditta A, Kaplan BB (2001) Local synthesis of nuclear-encoded mitochondrial proteins in the presynaptic nerve terminal. J Neurosci Res 64:447–453

    PubMed  CAS  Google Scholar 

  • Gioio AE, Scotto Lavina Z, Jurkovicova D, Eyman M, Giuditta A, Kaplan BB (2004) Nerve terminals of squid photoreceptor neurons contain a heterogeneous population of mRNAs and translate a transfected reporter mRNA. Eur J Neurosci 20:865–872

    PubMed  Google Scholar 

  • Giuditta A, Dettbarn WD, Brzin M (1968) Protein synthesis in the isolated giant axon of the squid. Proc Natl Acad Sci USA 59:1284–1287

    PubMed  CAS  Google Scholar 

  • Giuditta A, D'Udine B, Pepe M (1971) Uptake of protein by the giant axon of the squid. Nature 229:29–30

    CAS  Google Scholar 

  • Giuditta A, Cupello A, Lazzarini G (1980) Ribosomal RNA in the axoplasm of the squid giant axon. J Neurochem 34:1757–1760

    PubMed  CAS  Google Scholar 

  • Giuditta A, Hunt T, Santella L (1986) Messenger RNA in squid axoplasm. Neurochem Intern 8:435–442

    CAS  Google Scholar 

  • Giuditta A, Menichini E, Perrone Capano C, Langella M, Martin R, Castigli E, Kaplan BB (1991) Active polysomes in the axoplasm of the squid giant axon. J Neurosci Res 26:18–28

    Google Scholar 

  • Giuditta A, Kaplan BB, van Minnen J, Alvarez J, Koenig E (2002) Axonal and presynaptic protein synthesis: new insights into the biology of the neuron. Trends Neurosci 25:400–404

    PubMed  CAS  Google Scholar 

  • Giuditta A, Chun JT, Eyman M, Cefaliello C, Crispino M (2008) Local gene expression in axons and nerve endings: the glia-neuron unit. Physiol Rev 88:515–555

    PubMed  CAS  Google Scholar 

  • Grafstein B, Forman DS (1980) Intracellular transport in neurons. Physiol Rev 60:1167–1283

    PubMed  CAS  Google Scholar 

  • Grampp W, Edström JE (1963) The effect of nervous activity on ribonucleic acid of the crustacean receptor neuron. J Neurochem 10:725–731

    PubMed  CAS  Google Scholar 

  • Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139–143

    PubMed  CAS  Google Scholar 

  • Guan X, Clark GA (2006) Essential role of somatic and synaptic protein synthesis and axonal transport in long-term synapse-specific facilitation at distal sensomotor connections in Aplysia. Biol Bull 210:238–254

    PubMed  CAS  Google Scholar 

  • Hamberger A (1963) Difference between isolated neuronal and vascular glia with respect to respiratory activity. Acta Physiol Scand Suppl 58:1–58

    PubMed  CAS  Google Scholar 

  • Hamberger A, Hydén H (1963) Inverse enzymatic changes in neurons and glia during increased function and hypoxia. J Cell Biol 16:521–525

    PubMed  CAS  Google Scholar 

  • Hengst U, Jaffrey SR (2007) Function and translational regulation of mRNA in developing axons. Semin Cell Dev Biol 18:209–215

    PubMed  CAS  Google Scholar 

  • Hernandez AG, Langford GM, Martinez JL, Dowdall MJ (1976) Protein synthesis by synaptosomes from the head ganglion of the squid, Loligo pealli. Acta Cient Venez 27:120–123

    PubMed  CAS  Google Scholar 

  • Hillefors M, Gioio AE, Mameza MG, Kaplan BB (2007) Axon viability and mitochondrial function are dependent on local protein synthesis in sympathetic neurons. Cell Mol Neurobiol 27:701–716

    PubMed  CAS  Google Scholar 

  • Hirokawa N (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26:7139–7142

    PubMed  CAS  Google Scholar 

  • Holmgren E (1904) Ueber die trophospongien der nervenzellen. Anat Anz 24:225–244

    Google Scholar 

  • Holtzman E, Peterson ER (1969) Uptake of proteins by mammalian neurons. J Cell Biol 40:863–869

    PubMed  CAS  Google Scholar 

  • Hu JY, Meng X, Schacher S (2003) Redistribution of syntaxin mRNA in neuronal cell bodies regulates protein expression and transport during synapse formation and long-term synaptic plasticity. J Neurosci 23:1804–1815

    PubMed  CAS  Google Scholar 

  • Hu JY, Chen Y, Schacher S (2007) Protein kinase C regulates local synthesis and secretion of a neuropeptide required for activity-dependent long-term synaptic plasticity. J Neurosci 27:8927–8939

    PubMed  CAS  Google Scholar 

  • Huang HL, Cendan CM, Roza C, Okuse K, Cramer R, Timms JF, Wood JN (2008) Proteomic profiling of neuromas reveals alterations in protein composition and local protein synthesis in hyper-excitable nerves. Mol Pain 4:33

    PubMed  Google Scholar 

  • Hughes A, Flexner LB (1956) A study of the development of the cerebral cortex of the foetal guinea-pig by means of the ultraviolet microscope. J Anat 90:386–394

    PubMed  CAS  Google Scholar 

  • Hydén H, Egyházi E (1962a) Changes in the base composition of nuclear ribonucleic acid of neurons during a short period of enhanced protein production. J Cell Biol 15:37–44

    Google Scholar 

  • Hydén H, Egyházi E (1962b) Nuclear RNA changes of nerve cells during a learning experiment in rats. Proc Natl Acad Sci USA 48:1366–1373

    Google Scholar 

  • Hydén H, Egyházi E (1963) Glial RNA changes during a learning experiment in rats. Proc Natl Acad Sci USA 49:618–624

    PubMed  Google Scholar 

  • Hydén H, Egyházi E (1964) Changes in RNA content and base composition in cortical neurons of rats in a learning experiment involving transfer of handedness. Proc Natl Acad Sci USA 52:1030–1035

    PubMed  Google Scholar 

  • Hydén H, Egyházi E (1968) The effect of tranylcypromine on synthesis of macromolecules and enzyme activities in neurons and glia. Neurology 18:732–736

    PubMed  Google Scholar 

  • Hydén H, Lange PW (1965) A differentiation in RNA response in neurons early and late during learning. Proc Natl Acad Sci USA 53:946–952

    PubMed  Google Scholar 

  • Hydén H, Lange PW (1966) A genetic stimulation with production of adenic-uracil rich RNA in neurons and glia in learning. Naturwissen 53:64–70

    Google Scholar 

  • Hydén H, Pigon A (1960) A cytophysiological study of the functional relationship between oliodendroglial cells and nerve cells of Deiters' nucleus. J Neurochem 6:57–72

    PubMed  Google Scholar 

  • Ingoglia NA (1982) 4S RNA in regenerating optic axons of goldfish. J Neurosci 2:331–338

    PubMed  CAS  Google Scholar 

  • Jakoubek B, Edström JE (1965) RNA changes in the Mauthner axon and myelin sheath after increased functional activity. J Neurochem 12:845–849

    PubMed  CAS  Google Scholar 

  • Jimenez CJ, Eyman M, Scotto Lavina Z, Gioio AE, Li KW, van den Schors R, Geraerts WPM, Giuditta A, Kaplan BB, J van Minnen (2002) Protein synthesis in synaptosomes: a proteomic analysis. J Neurochem 81:735–744

    PubMed  CAS  Google Scholar 

  • Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406

    PubMed  CAS  Google Scholar 

  • Kaplan BB, Gioio AE, Perrone Capano C, Crispino M, Giuditta A (1992) β-actin and β-tubulin are components of a heterogeneous mRNA population present in the squid giant axon. Mol Cell Neurosci 3:133–144

    PubMed  CAS  Google Scholar 

  • Kaplan BB, Gioio AE, Hillefors M, Aschrafi A, (2009) Axonal Protein Synthesis and the Regulation of Local Mitochondrial Function. Results Probl Cell Differ. doi: 10.1007/400_2009_1

    Google Scholar 

  • Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685–690

    PubMed  CAS  Google Scholar 

  • Kindler S, Wang H, Richter D, Tiedge H (2005) RNA transport and local control of translation. Annu Rev Cell Dev Biol 21:223–245

    PubMed  CAS  Google Scholar 

  • Koenig E (1965) Synthetic mechanisms in the axon. II. RNA in myelin-free axons of the cat. J Neurochem 12:357–361

    CAS  Google Scholar 

  • Koenig E (1967) Synthetic mechanisms in the axon. IV. In vitro incorporation of [3H]precursors into axonal protein and RNA. J Neurochem 14:437–446

    PubMed  CAS  Google Scholar 

  • Koenig E (1979) Ribosomal RNA in Mauthner axon: implications for a protein synthesizing machinery in the myelinated axon. Brain Res 174:95–107

    PubMed  CAS  Google Scholar 

  • Koenig E, Giuditta A (1999) Protein synthesizing machinery in the axon compartment. Neuroscience 89:5–15

    PubMed  CAS  Google Scholar 

  • Kolodny GM (1971) Evidence for transfer of macromolecular RNA between mammalian cells in culture. Exp Cell Res 65:313–324

    PubMed  CAS  Google Scholar 

  • Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683–696

    PubMed  CAS  Google Scholar 

  • Kuffler SW, Nicholls JG (1966) The physiology of neuroglial cells. Ergeb Physiol 57:1–90

    PubMed  CAS  Google Scholar 

  • Kun A, Otero L, Sotelo-Silveira JR, Sotelo JR (2007) Ribosomal distribution in axons of mammalian myelinated fibers. J Neurosci Res 85:2087–2098

    PubMed  CAS  Google Scholar 

  • Landry CF, Campagnoni AT (1998) Targeting of mRNAs into neuronal and glial processes: intracellular and extracellular influences. Neuroscientist 4:77–87

    Google Scholar 

  • Lee JL (2008) Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11:1264–1266

    PubMed  CAS  Google Scholar 

  • Lee YS, Bailey CH, Kandel ER, Kaang BK (2008) Transcriptional regulation of long-term memory in the marine snail Aplysia. Mol Brain 1:3

    PubMed  Google Scholar 

  • Li YC, Li YN, Cheng CX, Sakamoto H, Kawate T, Shimada O, Atsumi S (2005) Subsurface cisterna-lined axonal invaginations and double-walled vesicles at the axonal-myelin sheath surface. Neurosci Res 53:298–303

    PubMed  CAS  Google Scholar 

  • Lieberman EM, Hargittai PT, Grossfeld RM (1994) Electrophysiological and metabolic interactions between axons and glia in crayfish and squid. Prog Neurobiol 44:333–376

    PubMed  CAS  Google Scholar 

  • Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89:312–323

    PubMed  CAS  Google Scholar 

  • Lugli G, Torvik VI, Larson J, Smalheiser NR (2008) Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J Neurochem 106:650–661

    PubMed  CAS  Google Scholar 

  • Lyles V, Zhao Y, Martin KC (2006) Synapse formation and mRNA localization in cultured Aplysia neuron. Neuron 49:349–356

    PubMed  CAS  Google Scholar 

  • Mariucci G, Giuditta A, Ambrosini MV (2007) Permanent brain ischemia induces marked increments in hsp72 expression and local protein synthesis in synapses of the ischemic hemisphere. Neurosci Lett 415:77–80

    PubMed  CAS  Google Scholar 

  • Martin KC (2004) Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 14:305–310

    PubMed  CAS  Google Scholar 

  • Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927–938

    PubMed  CAS  Google Scholar 

  • Martin KC, Zukin RS (2006) RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 26:7131–7134

    PubMed  CAS  Google Scholar 

  • Martin R, Vaida B, Bleher R, Crispino M, Giuditta A (1998) Protein synthesizing units in presynaptic and postsynaptic domains of squid neurons. J Cell Sci 111:3157–3166

    PubMed  CAS  Google Scholar 

  • Melia KR, Trembleau A, Oddi R, Sanna PP, Bloom FE (1994) Detection and regulation of tyrosine hydroxylase mRNA in catecholaminergic terminal fields: possible axonal compartmentalization. Exp Neurol 130:394–406

    PubMed  CAS  Google Scholar 

  • Menichini E, Castigli E, Kaplan BB, Giuditta A (1990) Synthesis of axoplasmic RNA particles in the isolated squid giant axon. Neurosc Res Commun 7:89–96

    CAS  Google Scholar 

  • Miller G (2005) The dark side of glia. Science 308:778–781

    PubMed  CAS  Google Scholar 

  • Miniaci MC, Kim JH, Puthanveettil SV, Si K, Zhu H, Kandel ER, Bailey CH (2008) Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron 59:1024–1036

    PubMed  CAS  Google Scholar 

  • Moccia R, Chen D, Lyles V, Kapuya E, Yaping E, Kalachikov S, Spahn CM, Frank J, Kandel ER, Barad M, Martin KC (2003) An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J Neurosci 23:9409–9417

    PubMed  CAS  Google Scholar 

  • Mohr E, Richter D (2000) Axonal mRNAs: functional significance in vertebrates and invertebrates. J Neurocytol 29:783–791

    PubMed  CAS  Google Scholar 

  • Morgan IG, Austin L (1968) Synaptosomal protein synthesis in a cell-free system. J Neurochem 15:41–51

    PubMed  CAS  Google Scholar 

  • Morgan IG, Austin L (1969) Ion effects and protein synthesis in synaptosomal fraction. J Neurobiol 2:155–167

    Google Scholar 

  • Motta CM, Castriota Scanderbeg M, Filosa S, Andreuccetti P (1995) Role of pyriform cells during the growth of oocytes in the lizard Podarcis sicula. J Exp Zool 273:247–256

    Google Scholar 

  • Murai KK, Van Meyel DJ (2007) Neuron glial communication at synapses: insights from vertebrates and invertebrates. Neuroscientist 13:657–666

    PubMed  Google Scholar 

  • Murashov AK, Chintalgattu V, Islamov RR, Lever TE, Pak ES, Sierpinski PL, Katwa LC, Van Scott MR (2007) RNAi pathway is functional in peripheral nerve axons. FASEB J 21:656–670

    PubMed  CAS  Google Scholar 

  • Muslimov IA, Titmus M, Koenig E, Tiedge H (2002) Transport of neuronal BC1 RNA in Mauthner axons. J Neurosci 22:4293–4301

    PubMed  CAS  Google Scholar 

  • Newman EA (2003) New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 26:536–542

    PubMed  CAS  Google Scholar 

  • Perrone Capano C, Giuditta A, Castigli E, Kaplan BB (1987) Occurrence and sequence complexity of polyadenylated RNA in squid axoplasm. J Neurochem 49:698–704

    CAS  Google Scholar 

  • Pevzner LZ (1965) Topochemical aspects of nucleic acid and protein metabolism within the neuron-neuroglia unit of the superior cervical ganglion. J Neurochem 12:993–1002

    PubMed  CAS  Google Scholar 

  • Pevzner LZ (1971) Topochemical aspects of nucleic acid and protein metabolism within the neuron-neuroglia unit of the spinal cord anterior horn. J Neurochem 18:895–907

    PubMed  CAS  Google Scholar 

  • Piper M, Holt C (2004) RNA translation in axons. Annu Rev Cell Dev Biol 20:505–523

    PubMed  CAS  Google Scholar 

  • Por S, Gunning PW, Jeffrey PL, Austin L (1978) Axonal transport of 4S RNA in the chick optic system. Neurochem Res 3:411–422

    PubMed  CAS  Google Scholar 

  • Puthanveettil SV, Monje FJ, Miniaci MC, Choi YB, Karl KA, Khandros E, Gawinowicz MA, Sheetz MP, Kandel ER (2008) A new component in synaptic plasticity: upregulation of Kinesin in the neurons of the gill withdrawal reflex. Cell 135:960–973

    PubMed  CAS  Google Scholar 

  • Rapallino MV, Cupello A, Giuditta A (1988) Axoplasmic RNA species synthesized in the isolated squid giant axon. Neurochem Res 13:625–631

    PubMed  CAS  Google Scholar 

  • Reichenbach A, Pannicke T (2008) Neuroscience. A new glance at glia. Science 2008 322:693–694

    CAS  Google Scholar 

  • Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH (2004) Nanotubular highways for intercellular organelle transport. Science 303:1007–1010

    PubMed  CAS  Google Scholar 

  • Schacher S, Wu F, Panyko JD, Sun Z-Y, Wang D (1999) Expression and branch-specific export of mRNA are regulated by synapse formation and interaction with specific postsynaptic targets. J Neurosci 19:6338–6347

    PubMed  CAS  Google Scholar 

  • Si K, Lindquist S, Kandel ER (2003a) A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell 115:879–891

    CAS  Google Scholar 

  • Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, Miniaci MC, Kim JH, Zhu H, Kandel ER (2003b) A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell 115:893–904

    CAS  Google Scholar 

  • Singer M, Green M (1968) Autoradiographic studies of uridine incorporation in peripheral nerve of the newt, Triturus. J Morphol 124:321–344

    PubMed  CAS  Google Scholar 

  • Slagel DE, Hartman HA, Edström JE (1966) The effect of iminodiproprionitrile on the ribonucleic acid content and composition of mesencephalic V cells, anterior horn cells, glial cells, and axonal balloons. J Neuropathol Exp Neurol 25:244–253

    PubMed  CAS  Google Scholar 

  • Smith C, Kelly G (1988) Paradoxical sleep deprivation applied two days after end of training retards learning. Physiol Behav 43:213–216

    PubMed  CAS  Google Scholar 

  • Sotelo-Silveira JR, Calliari A, Kun A, Koenig E, Sotelo JR (2006) RNA trafficking in axons. Traffic 7:508–515

    PubMed  CAS  Google Scholar 

  • Spencer GE, Syed NI, van Kesteren E, Lucowiak K, Geraerts WPM, van Minnen J (2000) Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J Neurobiol 44:72–81

    PubMed  CAS  Google Scholar 

  • Steward O, Banker GA (1992) Getting the message from the gene to the synapse: sorting and intracellular transport of RNA in neurons. Trends Neurosci 15:180–186

    PubMed  CAS  Google Scholar 

  • Thoenen H, Mueller RA, Axelrod J (1970) Phase difference in the induction of tyrosine hydroxylase in cell body and nerve terminals of sympathetic neurones. Proc Natl Acad Sci USA 65:58–62

    PubMed  CAS  Google Scholar 

  • Tobias GS, Koenig E (1975) Influence of nerve cell body and neurolemma cell on local axonal protein synthesis following neurotomy. Exp Neurol 49:235–245

    PubMed  CAS  Google Scholar 

  • Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    PubMed  CAS  Google Scholar 

  • van Minnen J (1994) RNA in the axonal domain: a new dimension in neuronal functioning? Histochem J 26:377–391

    PubMed  Google Scholar 

  • van Minnen J, Bergman JJ, van Kesteren ER, Smit AB, Geraerts WPM, Lukowiak K, Hasan SU, Syed NI (1997) De novo protein synthesis in isolated axons of identified neurons. Neuroscience 80:1–7

    PubMed  Google Scholar 

  • Verity MA, Brown WJ, Cheung MK (1979) On the mechanism of ouabain inhibition of synaptosome protein synthesis. J Neurochem 32:1295–1301

    PubMed  CAS  Google Scholar 

  • Vincent JP, Magee T (2002) Argosomes: membrane fragments on the run. Trends Cell Biol 12:57–60

    PubMed  CAS  Google Scholar 

  • Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Rev Neurosci 6:626–640

    CAS  Google Scholar 

  • Vuppalanchi et al. (2009) Results Probl Cell Differ

    Google Scholar 

  • Watson WE (1974) Physiology of neuroglia. Physiol Rev 54:245–271

    PubMed  CAS  Google Scholar 

  • Whittaker VP (1993) Thirty years of synaptosome research. J Neurocytol 22:735–742

    PubMed  CAS  Google Scholar 

  • Willis DE, Li KW, Zheng J-Q, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurogeneration protein mRNAs in axons. J Neurosci 26:778–791

    Google Scholar 

  • Willis DE, Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL (2007) Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 178:965–980

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonio Giuditta .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Crispino, M., Cefaliello, C., Kaplan, B., Giuditta, A. (2009). Protein Synthesis in Nerve Terminals and the Glia–Neuron Unit. In: Koenig, E. (eds) Cell Biology of the Axon. Results and Problems in Cell Differentiation, vol 48. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2009_9

Download citation

Publish with us

Policies and ethics