Abstract
To get insight into the stimulus-dependent translocation of mRNA encoding neuropeptides to the axonal compartment of neurons, we investigated this process in the egg-laying hormone producing caudodorsal cells of the mollusk Lymnaea stagnalis. The axonal compartment including the nerve terminals of these neurons harbors high amounts of mRNA encoding the egg-laying hormone precursor. We determined how a sensory stimulus, that results in egg-laying, affected the amount of egg-laying hormone encoding transcripts in the axon endings. Four hours after stimulation high amounts of transcripts were detected in the axonal compartment and maximum values were reached after 8 h. Transcript levels in the somata were affected in a similar fashion, although the increase was not as pronounced as in the axons. Next, we investigated the ultrastructural localization of egg-laying hormone encoding transcripts in axons and axon terminals by means of electron microscopic in situ hybridization and showed that transcripts were localized in the axoplasm. By means of conventional electron microscopy we showed that axon terminals of egg-laying hormone producing neurons contained large amounts of polyribosomes. Together, these data support the notion that egg-laying hormone encoding transcripts are translated in the axonal compartment.
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Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013–1026
Crispino M, Capano CP, Kaplan BB, Giuditta A (1993) Neurofilament proteins are synthesized in nerve endings from squid brain. J Neurochem 61:1144–1146
Dirks RW, Van Dorp AGM, Van Minnen J, Fransen JAM, Van der Ploeg M, Raap AK (1993) Ultrastructural evidence for the axonal localization of caudodorsal cell mRNA in the central nervous system of the mollusc Lymnaea stagnalis. Microsc Res and Tech 25:12–18
Gardiol A, Racca C, Triller A (1999) Dendritic and postsynaptic protein synthetic machinery. J Neurosci 19:168–179
Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Science 336:674–677
Geraerts WPM, Ter Maat A, Vreugdenhil E (1988) The peptidergic neuroendocrine control of egg-laying behavior in Aplysia and Lymnaea. In: Laufer H, Downer RGH (eds) Invertebrate endocrinology, vol 2. Liss, New York, pp 144–231
Ginzburg I (1991) Neuronal polarity: targeting of microtubule components into axons and dendrites. Trends Biochem Sci 16:257–261
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
Giuditta A, Metafora S, Felsani A, Del Rio A (1977) Factors for protein synthesis in the axoplasm of squid giant axons. J Neurochem 28:1391–1395
Hu J-H, Meng X, Schacher S (2002) Target interaction regulates distribution and stability of specific mRNAs. J Neurosci 22:2669–2678
Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406
Kaplan BB, Gioio AE, Perrone Capano C, Crispino M, Giuditta A (1992) Beta-actin and beta-tubulin are components of a heterogeneous mRNA population present in the squid giant axon. Mol Cell Neurosci 3:133–144
Kiebler MA, Hemraj IA, Verkade P, Kohrmann M, Fortes P, Marion RM, Ortin J, Dotti CG (1999) The mammalian Staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J Neurosci 19:288–297
Klumperman J, Spijker S, Van Minnen J, Sharp-Baker H, Smit AB, Geraerts WPM (1996) Cell type-specific sorting of neuropeptides: a mechanism to modulate peptide composition of large dense-core vesicles. J Neurosci 16:7930–7940
Martin KC, Casidio A, et al (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
Martin KC, Barad M, Kandel ER (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr Opin Neurobiol 10:587–592
Melton DA (1987) Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328:80–82
Miyashiro K, Dichter M, Eberwine J (1994) On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc Natl Acad Sci U S A 91:10800–10804
Mohr E, Fehr S, Richter D (1991) Axonal transport of neuropeptide encoding messenger RNAs within the hypothalamohypophyseal tract of rats. EMBO J 10:2419–2424
Roubos EW (1984) Cytobiology of the ovulation-neurohormone producing caudodorsal cells of the snail Lymnaea stagnalis. Int Rev Cytol 89:295–346
Schacher S, Wu F, Panyko JD, Sun ZY, 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
Shestakova EA, Singer RH, Condeelis J (2001) The physiological significance of beta-actin mRNA localization in determining cell polarity and directional motility. Proc Natl Acad Sci U S A 98:7045–7050
Spencer GE, Syed NI, Kesteren E van, Lukowiak K, Geraerts WP, Minnen J van (2000) Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J Neurobiol 44:72–81
Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localise selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751
Stjohnston D (1995) The intracellular localization of messenger RNAs. Cell 81:161–170
Ter Maat A, Lodder JC, Wilbrink M (1983) Induction of egg laying in the pond snail Lymnaea stagnalis by environmental stimulation of the release of ovulation hormone from the caudodorsal cells. Int J Invert Reprod 6:239–247
Tiedge H, Brosius J (1996) Translational machinery in dendrites of hippocampal neurons in culture. J Neurosci 16:7171–7181
Uhl GR, Evans J, Parta M, Walworth C, Hill K, Sasek C, Voigt M, Reppert S (1986) Vasopressin and somatostatin mRNA. In: Uhl GR (ed) In situ hybridization in the brain. Plenum Press, New York, pp 21–47
Van Minnen J (1994a) RNA in the axonal domain: a new dimension in neuronal functioning? Histochem J 26:377–391
Van Minnen J (1994b) Axonal localization of neuropeptide-encoding mRNA in identified neurons of the snail Lymnaea stagnalis. Cell Tissue Res 276:155–161
Van Minnen J, Bergman JJ, Van Kesteren ER, Smit AB, Geraerts WP, Lukowiak K, Hasan SU, Syed NI (1997) De novo protein synthesis in isolated axons of identified neurons. Neuroscience 80:1–7
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van Minnen, J., Bergman, J.J. Stimulus-dependent translocation of egg-laying hormone encoding mRNA into the axonal compartment of the neuroendocrine caudodorsal cells. Invert Neurosci 5, 1–7 (2003). https://doi.org/10.1007/s10158-003-0022-4
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DOI: https://doi.org/10.1007/s10158-003-0022-4