Subcellular localization of preprogalanin messenger RNA in perikarya and axons of hypothalamo-posthypophyseal magnocellular neurons: An in situ hybridization study

Neuroscience

Volumn 84, Issue 3, 1998, Pages 897-912

  Landry, M ^a   Hokfelt T ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Axonal mRNA transport; Electron microscopy; Galanin; Median eminence; Neuropeptides; Salt loading

Indexed keywords

GALANIN; MESSENGER RNA; OXYTOCIN; VASOPRESSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR TRANSPORT; MALE; MESSENGER RNA SYNTHESIS; NONHUMAN; OXYTOCIN RELEASE; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; VASOPRESSIN RELEASE;

ANIMALS; AXONS; DENDRITES; DIGOXIGENIN; GALANIN; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICROSCOPY, ELECTRON; NEURONS; OLIGONUCLEOTIDE PROBES; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUBCELLULAR FRACTIONS;

EID: 0032562174     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00567-8     Document Type: Article

References (82)

1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 101:1987;1-22.
2. Arai R., Onteniente B., Trembleau A., Landry M., Calas A. Hypothalamic galanin-immunoreactive neurons projecting to the posterior lobe of the rat pituitary: a combined retrograde tracing and immunohistochemical study. J. comp. Neurol. 299:1990;405-420.
3. Berleth T., Burri M., Thoma G., Bopp D., Richstein S., Frigerio G., Noll M., Nüsslein-Volhard C. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. Eur. molec. Biol. Org. J. 7:1988;1749-1756.
4. Bian F., Chu T., Schilling K. Differential mRNA transport and the regulation of protein synthesis: selective sensitivity of Purkinje cell dendritic mRNAs to translational inhibition. Molec. cell. Neurosci. 7:1996;116-133.
5. Bloch B., Guitteny A. F., Normand E., Chouham S. Presence of neuropeptide messenger RNAs in neuronal processes. Neurosci. Lett. 109:1990;259-264.
6. Boyer P. A., Trembleau A., Leviel V., Arluison M. Effects of intranigral injections of colchicine on the expression of some neuropeptides in the rat forebrain: an in situ hybridization study. Brain Res. Bull. 33:1994;541-560.
7. Brophy P. J., Boccacio G. L., Colman D. R. The distribution of myelin basic protein mRNAs within myelinating oligodendrocytes. Trends Neurosci. 16:1993;515-521.
8. Brownstein M. J. and Mezey E. (1986) Multiple chemical messengers in hypothalamic magnocellular neurons. In Progress in Brain Research (eds Hökfelt T., Fuxe K. and Pernow B.), Vol. 68, pp. 161-168. Elsevier, Amsterdam.
9. 2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 10:1990;1788-1798.
10. Cortés R., Ceccatelli S., Schalling M., Hökfelt T. Differential effects of intracerebroventricular colchicine administration on the expression of mRNAs for neuropeptides and neurotransmitter enzymes, with special emphasis on galanin: an in situ hybridization study. Synapse. 6:1990;369-391.
11. Dagerlind Å., Friberg K., Bean A., Hökfelt T. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry. 98:1992;39-49.
12. Davis L., Banker G. A., Steward O. Selective dendritic transport of RNA in hippocampal neurons in culture. Nature. 330:1987;477-479.
13. Driever W., Nüsslein-Volhard C. A gradient of bicoid protein in Drosophila embryo. Cell. 54:1988;83-93.
14. Fontaine B., Sassoon D., Buckingham M., Changeux J. P. Detection of the nicotinic acetylcholine receptor α-subunit mRNA, in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. Eur. molec. Biol. Org. J. 7:1988;603-609.
15. Furuichi T., Simon-Chazottes D., Fujino I., Yamada N., Hasegawa M., Miyawaki A., Yoshawa S., Guenet J. L., Mikosha K. Widespread expression of inositol 1,4,5-triphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. Receptors Channels. 1:1993;11-24.
16. Garner C. C., Tucker R. P., Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature. 336:1988;674-677.
17. Gavis E. R., Lehmann R. Localization of nanos RNA controls embryonic polarity. Cell. 71:1992;310-313.
18. Gaymann W., Martin R. Immunoreactive galanin-like material in magnocellular hypothalamo-neurohypophyseal neurons of the rat. Cell Tiss. Res. 255:1989;139-147.
19. Gottlieb E. Messenger RNA transport and localization. Curr. Opin. Cell Biol. 2:1990;1080-1086.
20. Gottlieb E. The 3′ untranslated regions of localized maternal messages contains a conserved motif involved in mRNA localization. Proc. natn. Acad. Sci. U.S.A. 89:1992;7164-7168.
21. Guitteny A. F., Bloch B. Ultrastructural detection of vasopressin messenger RNA in the normal and Brattleboro rat. Histochemistry. 92:1989;277-281.
22. Jirikowski G. F., Sanna P. P., Bloom F. E. mRNA coding oxytocin is present in axons of the hypothalamo-neurohypophyseal tract. Proc. natn. Acad. Sci. U.S.A. 87:1990;7400-7404.
23. Kaplan L. M., Spindel E. R., Isselbacher K. J., Chin W. W. Tissue-specific expression of the rat galanin gene. Proc. natn. Acad. Sci. U.S.A. 85:1988;1065-1069.
24. Kerstens H. M. J., Poddighe P. J., Hanselaar A. G. J. M. A novel in situ hybridization signal amplification method based on the deposition of biotinylated tyramine. J. Histochem. Cytochem. 43:1995;347-352.
25. Kislauskis E. H., Li Z., Singer R. H., Taneja K. L. Isoform-specific 3′-untranslated sequences sort α-cardiac and b-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. J. Cell Biol. 123:1993;165-172.
26. Kislauskis E. H., Singer R. H. Determinants of mRNA localization. Curr. Opin. Cell Biol. 4:1992;975-978.
27. Kondo K., Murase T., Otake K., Ito M., Oiso Y. Centrally administered galanin inhibits osmotically stimulated arginine vasopressin release in conscious rats. Neurosci. Lett. 128:1991;245-248.
28. Landry C. F., Watson J. B., Kashima T., Campagnoni A. T. Cellular influences on RNA sorting in neurons and glia: an in situ hybridization histochemical study. Molec. Brain Res. 27:1994;1-11.
29. Landry M., Roche D., Calas A. Short term effects of centrally administered galanin on the hyperosmotic stimulated expression of vasopressin in the rat hypothalamus. An in situ and immunohistochemistry study. Neuroendocrinology. 61:1995;393-404.
30. Landry M., Trembleau A., Arai R., Calas A. Evidence for a colocalization of oxytocin mRNA and galanin in magnocellular hypothalamic neurons: a study combining in situ hybridization and immunohistochemistry. Molec. Brain Res. 10:1991;91-95.
31. Lawrence J. B., Singer R. H. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cells. 45:1986;407-415.
32. Levy A., Lightman S. L., Carter D. A., Murphy D. The origin and regulation of posterior pituitary vasopressin ribonucleic acid in osmotically stimulated rats. J. Neuroendocr. 2:1990;329-334.
33. Luby-Phelps K. Effect of cytoarchitecture on the transport and localization of protein synthetic machinery. J. Cell Biochem. 52:1993;140-147.
34. Meister B., Cortés R., Villar M. J., Schalling M., Hökfelt T. Peptides and transmitter enzymes in hypothalamic magnocellular neurons after administration of hyperosmotic stimuli: comparison between messenger RNA and peptide/protein levels. Cell Tiss. Res. 260:1990;279-297.
35. Melander T., Hökfelt T., Rökaeus Å. Distribution of galanin-like immunoreactivity in the rat central nervous system. J. comp. Neurol. 248:1986;475-517.
36. Melander T., Hökfelt T., Rökaeus Å., Cuello A. C., Oertel W. H., Verhofstad A., Goldstein M. Coexistence of galanin-like immunoreactivity with catecholamines, 5-hydroxytryptamine, GABA and neuropeptides in the rat CNS. J. Neurosci. 6:1986;3640-3654.
37. Melton D. A. Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature. 328:1987;80-82.
38. Melton D. A. Pattern formation during animal development. Science. 252:1991;234-241.
39. Merlie J. P., Sanes J. R. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibers. Nature. 317:1985;66-68.
40. Miyashiro K., Dichter M., Eberwine J. On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. natn. Acad. Sci. U.S.A. 91:1994;10800-10804.
41. Mohr E., Fehr S., Richter D. Axonal transport of neuropeptide encoding mRNAs within the hypothalamo-hypophyseal tract of rats. Eur. molec. Biol. Org. J. 10:1991;2419-2424.
42. Mohr E., Morris J. F., Richter D. Differential subcellular mRNA targeting: deletion of a single nucleotide prevents the transport to axons but not to dendrites of rat hypothalamic magnocellular neurons. Proc. natn. Acad. Sci. U.S.A. 92:1995;4377-4381.
43. Mohr E., Richter D. Diversity of mRNAs in the axonal compartment of peptidergic neurons in the rat. Eur. J. Neurosci. 4:1992;870-876.
44. Morris J. F. Distribution of neurosecretory granules among the anatomical compartments of the neurosecretory processes of the pituitary gland: a quantitative ultrastructural approach to hormone storage in the neuronal lobe. J. Endocr. 68:1976;225-234.
45. Morris J. F., Pow D. V., Sokol H. W. and Ward A. (1993) Dendritic release of peptides from magnocellular neurons in normal rats, Brattleboro rats and mice with hereditary nephrogenic diabetes insipidus. In Vasopressin (eds Gross P., Richter D. and Robertson G. L.), pp. 171-182. John Libbey Eurotext, Paris.
46. Murphy D., Levy A., Lightman S., Carter D. Vasopressin mRNA in the neural lobe of the pituitary: dramatic accumulation in response to salt-loading. Proc. natn. Acad. Sci. U.S.A. 86:1989;9002-9005.
47. Nüsslein-Volhard C., Frohnhöfer H. G., Lehmann R. Determination of anteroposterior polarity in Drosophila. Science. 238:1987;1675-1681.
48. Pease P. C. Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142:1962;342.
49. Pow D. V., Morris J. F. Dendrites of hypothalamic magnocellular neurons release neurophypophysial peptides by exocytosis. Neuroscience. 32:1989;435-439.
50. Prakash N., Fehr S., Mohr E., Richter D. Dendritic localization of rat vasopressin mRNA: ultrastructural analysis and mapping of targeting elements. Eur. J. Neurosci. 9:1997;523-532.
51. Racca C., Gardiol A., Triller A. Dendritic and postsynaptic localizations of glycine receptor α subunit mRNAs. J. Neurosci. 17:1997;1691-1700.
52. Rapp A. K., van de Corput M. P. C., Vervenne R. A. W., van Gijlswijk R. P. M., Tanke H. J., Wiegant J. Ultra-sensitive FISH using peroxidase-mediated deposition of biotin or fluorochrome tyramides. Hum. molec. Genet. 4:1995;529-534.
53. Rökaeus Å., Young I. W. S., Mezey E. Galanin coexists with vasopressin in the normal rat hypothalamus and galanin's synthesis is increased in the Brattleboro (diabetes insipidus) rat. Neurosci. Lett. 90:1988;45-50.
54. Schmitz G. G., Walter T., Seibl R., Kessler C. Nonradioactive labeling of oligonucleotides in vitro with the hapten digoxigenin by tailing with terminal transferase. Ann. Biochem. 192:1991;222-231.
55. Skofitsch G., Jacobowitz D. M. Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides. 6:1985;509-546.
56. Skofitsch G., Jacobowitz D. M., Amann R., Lembeck F. Galanin and vasopressin coexist in the rat hypothalamo-neurohypophyseal system. Neuroendocrinology. 49:1989;419-427.
57. Sofroniew M. W. (1985) Vasopressin, oxytocin and their related neurophysins. In Handbook of Chemical Neuroanatomy. GABA and Neuropeptides in the CNS, Part 4 (eds Björklund A. and Hökfelt T.), pp. 93-165. Elsevier, Amsterdam.
58. Steward O. Targeting of mRNAs to subsynaptic microdomains in dendrites. Curr. Opin. Neurobiol. 5:1995;55-61.
59. Steward O., Banker G. A. Getting the message from the gene to the synapse: sorting and intracellular transport of RNA in neurons. Trends Neurosci. 15:1992;180-186.
60. Steward O., Levy W. B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 2:1982;284-291.
61. Steward O., Reeves T. M. Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J. Neurosci. 8:1988;176-184.
62. St. Johnston D. The intracellular localization of messenger RNAs. Cell. 81:1995;161-170.
63. Sundell C. L., Singer R. H. Requirement of microfilaments in sorting of actin messenger RNA. Science. 253:1991;1275-1277.
64. Tiedge H., Zhou A., Brosius N. A. T. Transport of BC1 RNA in hypothalamo-neurohypophyseal axons. J. Neurosci. 13:1993;4214-4219.
65. Torre E. R., Steward O. 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. 12:1992;762-772.
66. Torre E. R., Steward O. Protein synthesis within dendrites: glycosylation of newly synthesized proteins in dendrites from their cell bodies. J. Neurosci. 16:1996;5967-5978.
67. Trembleau A., Bloom F. E. Enhanced sensitivity for light and electron microscopic in situ hybridization with multiple simultaneous non-radioactive oligodeoxynucleotide probes. J. Histochem. Cytochem. 43:1995;829-841.
68. αS mRNA and vasopressin mRNA to distinct domains of the rough endoplasmic reticulum within secretory neurons of the rat hypothalamus. Molec. cell. Neurosci. 7:1996;17-28.
69. Trembleau A., Calas A., Fèvre-Mongagne M. Ultrastructural localization of oxytocin mRNA in the rat hypothalamus by in situ hybridization using a synthetic oligonucleotide. Molec. Brain Res. 8:1990;37-45.
70. Trembleau A., Melia K. R., Bloom F. E. BC1 RNA and vasopressin mRNA in rat neurohypophysis: axonal compartmentalization and differential regulation during dehydration and rehydration. Eur. J. Neurosci. 7:1995;2249-2260.
71. 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. 14:1994;39-53.
72. Trembleau A., Morales M., Bloom F. E. Differential compartmentalization of vasopressin messenger RNA and neuropeptide within the rat hypothalamo-neurohypophysial axonal tracts: light and electron microscopic evidence. Neuroscience. 70:1996;113-125.
73. van Gijlswijk R. P. M., Wiegant J., Raap A. K., Tanke H. J. Improved localization of fluorescent tyramides for fluorescence in situ hybridization using dextran sulfate and polyvinyl alcohol. J. Histochem. Cytochem. 44:1996;389-392.
74. van Leeuwen F. W. Mutant vasopressin precursor producing cells of the homozygous Brattleboro rat hypothalamus. Proc. natn. Acad. Sci. U.S.A. 82:1992;149-155.
75. Villar M. J., Meister B., Cortés R., Schalling M., Morris M., Hökfelt T. Neuropeptide gene expression in hypothalamic magnocellular neurons of normal and hypophysectomized rats: a combined immunohistochemical and in situ hybridization study. Neuroscience. 36:1990;181-199.
76. Wang H., Ward A. R., Morris J. F. Oestradiol acutely stimulates exocytosis of oxytocin and magnocellular neurons. Neuroscience. 68:1995;1179-1188.
77. Wilhelm J. E., Vale R. D. RNA on the move: the mRNA localization pathway. J. Cell Biol. 123:1993;269-274.
78. Yisraeli J. K., Melton D. A. The maternal mRNA Vg1 is correctly localized following injection into Xenopus oocytes. Nature. 336:1988;592-595.
79. Yisraeli J. K., Sokol S., Melton D. A. A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development. 108:1990;289-298.
80. Young W. S., Horváth S., Palkovits M. The influences of hyperosmolality and synaptic inputs on galanin and vasopressin expression in the hypothalamus. Neuroscience. 39:1990;115-125.
81. Young W. S. Simultaneous use of digoxigenin and radiolabeled oligodeoxyribonucleotide probes. Neuropeptides. 13:1989;271-275.
82. Young W. S. (1990) In situ hybridization histochemistry. In Handbook of Chemical Neuroanatomy (eds Björklund A., Hökfelt T., Wouterlood F. G. and Van den Pol A. N.), pp. 481-512. Elsevier, Amsterdam.