Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 May 9;92(10):4377–4381. doi: 10.1073/pnas.92.10.4377

Differential subcellular mRNA targeting: deletion of a single nucleotide prevents the transport to axons but not to dendrites of rat hypothalamic magnocellular neurons.

E Mohr 1, J F Morris 1, D Richter 1
PMCID: PMC41947  PMID: 7753814

Abstract

It has previously been shown that mRNA encoding the arginine vasopressin (AVP) precursor is targeted to axons of rat magnocellular neurons of the hypothalamo-neurohypophyseal tract. In the homozygous Brattle-boro rat, which has a G nucleotide deletion in the coding region of the AVP gene, no such targeting is observed although the gene is transcribed. RNase protection and heteroduplex analyses demonstrate that, in heterozygous animals, which express both alleles of the AVP gene, the wild-type but not the mutant transcript is subject to axonal compartmentation. In contrast, wild-type and mutant AVP mRNAs are present in dendrites. These data suggest the existence of different mechanisms for mRNA targeting to the two subcellular compartments. Axonal mRNA localization appears to take place after protein synthesis; the mutant transcript is not available for axonal targeting because it lacks a stop codon preventing its release from ribosomes. Dendritic compartmentation, on the other hand, is likely to precede translation and, thus, would be unable to discriminate between the two mRNAs.

Full text

PDF
4377

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bloch B., Guitteny A. F., Normand E., Chouham S. Presence of neuropeptide messenger RNAs in neuronal processes. Neurosci Lett. 1990 Feb 16;109(3):259–264. doi: 10.1016/0304-3940(90)90004-s. [DOI] [PubMed] [Google Scholar]
  2. Burgin K. E., Waxham M. N., Rickling S., Westgate S. A., Mobley W. C., Kelly P. T. In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain. J Neurosci. 1990 Jun;10(6):1788–1798. doi: 10.1523/JNEUROSCI.10-06-01788.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dugich-Djordjevic M. M., Tocco G., Willoughby D. A., Najm I., Pasinetti G., Thompson R. F., Baudry M., Lapchak P. A., Hefti F. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron. 1992 Jun;8(6):1127–1138. doi: 10.1016/0896-6273(92)90133-x. [DOI] [PubMed] [Google Scholar]
  4. Garner C. C., Tucker R. P., Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature. 1988 Dec 15;336(6200):674–677. doi: 10.1038/336674a0. [DOI] [PubMed] [Google Scholar]
  5. Jeannotte L., Burbach J. P., Drouin J. Unusual proopiomelanocortin ribonucleic acids in extrapituitary tissues: intronless transcripts in testes and long poly(A) tails in hypothalamus. Mol Endocrinol. 1987 Oct;1(10):749–757. doi: 10.1210/mend-1-10-749. [DOI] [PubMed] [Google Scholar]
  6. Jirikowski G. F., Sanna P. P., Bloom F. E. mRNA coding for oxytocin is present in axons of the hypothalamo-neurohypophysial tract. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7400–7404. doi: 10.1073/pnas.87.19.7400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kew D., Jin D. F., Kim F., Laddis T., Kilpatrick D. L. Translational status of proenkephalin mRNA in the rat reproductive system. Mol Endocrinol. 1989 Aug;3(8):1191–1196. doi: 10.1210/mend-3-8-1191. [DOI] [PubMed] [Google Scholar]
  8. Lasek R. J., Brady S. T. The axon: a prototype for studying expressional cytoplasm. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):113–124. doi: 10.1101/sqb.1982.046.01.015. [DOI] [PubMed] [Google Scholar]
  9. Miyashiro K., Dichter M., Eberwine J. On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10800–10804. doi: 10.1073/pnas.91.23.10800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mohr E., Fehr S., Richter D. Axonal transport of neuropeptide encoding mRNAs within the hypothalamo-hypophyseal tract of rats. EMBO J. 1991 Sep;10(9):2419–2424. doi: 10.1002/j.1460-2075.1991.tb07781.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mohr E., Zhou A., Thorn N. A., Richter D. Rats with physically disconnected hypothalamo-pituitary tracts no longer contain vasopressin-oxytocin gene transcripts in the posterior pituitary lobe. FEBS Lett. 1990 Apr 24;263(2):332–336. doi: 10.1016/0014-5793(90)81407-f. [DOI] [PubMed] [Google Scholar]
  12. Mohr Evita, Richter Dietmar. Diversity of mRNAs in the Axonal Compartment of Peptidergic Neurons in the Rat. Eur J Neurosci. 1992;4(9):870–876. doi: 10.1111/j.1460-9568.1992.tb00197.x. [DOI] [PubMed] [Google Scholar]
  13. Pow D. V., Morris J. F. Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience. 1989;32(2):435–439. doi: 10.1016/0306-4522(89)90091-2. [DOI] [PubMed] [Google Scholar]
  14. Pow D. V., Morris J. F., Rodgers S. Peptide accretions in the endoplasmic reticulum of magnocellular neurosecretory neurons in normal and experimentally manipulated rats. J Anat. 1991 Oct;178:155–174. [PMC free article] [PubMed] [Google Scholar]
  15. Pow D. V., Morris J. F., Ward A. R. Immuno-electron microscopic evidence for two different types of partial somatic repair of the mutant Brattleboro vasopressin gene. Neuroscience. 1992 Oct;50(3):503–512. doi: 10.1016/0306-4522(92)90442-5. [DOI] [PubMed] [Google Scholar]
  16. Schmale H., Ivell R., Breindl M., Darmer D., Richter D. The mutant vasopressin gene from diabetes insipidus (Brattleboro) rats is transcribed but the message is not efficiently translated. EMBO J. 1984 Dec 20;3(13):3289–3293. doi: 10.1002/j.1460-2075.1984.tb02291.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Skutella T., Probst J. C., Blanco E., Jirikowski G. F. Localization of tyrosine hydroxylase mRNA in the axons of the hypothalamo-neurohypophysial system. Brain Res Mol Brain Res. 1994 Apr;23(1-2):179–184. doi: 10.1016/0169-328x(94)90224-0. [DOI] [PubMed] [Google Scholar]
  18. Steward O. Dendrites as compartments for macromolecular synthesis. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10766–10768. doi: 10.1073/pnas.91.23.10766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Steward O., Levy W. B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci. 1982 Mar;2(3):284–291. doi: 10.1523/JNEUROSCI.02-03-00284.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tiedge H., Fremeau R. T., Jr, Weinstock P. H., Arancio O., Brosius J. Dendritic location of neural BC1 RNA. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2093–2097. doi: 10.1073/pnas.88.6.2093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tiedge H., Zhou A., Thorn N. A., Brosius J. Transport of BC1 RNA in hypothalamo-neurohypophyseal axons. J Neurosci. 1993 Oct;13(10):4214–4219. doi: 10.1523/JNEUROSCI.13-10-04214.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Trembleau A., Morales M., Bloom F. E. Aggregation of vasopressin mRNA in a subset of axonal swellings of the median eminence and posterior pituitary: light and electron microscopic evidence. J Neurosci. 1994 Jan;14(1):39–53. doi: 10.1523/JNEUROSCI.14-01-00039.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES