Differential routing of coexisting neuropeptides in vasopressin neurons

European Journal of Neuroscience

Volumn 17, Issue 11, 2003, Pages 579-589

  Landry, Marc ^a   Vila Porcile, Evelyne ^b   Hökfelt, Tomas ^c   Calas, André ^b  

^a INSERM   (France)

^b CNRS   (France)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Electron microscopy; Galanin; Hypothalamus; Intracellular targeting; Neuropeptide; Rat; Vasopressin

Indexed keywords

GALANIN; MESSENGER RNA; NEUROPEPTIDE; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CELL COUNT; CELL LABELING; CELL POPULATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; ENDOCRINE FUNCTION; ENDOPLASMIC RETICULUM; GRANULE CELL; HYPOPHYSIS; HYPOTHALAMUS; IMMUNOGOLD LABELING; IMMUNOLOCALIZATION; IN SITU HYBRIDIZATION; INTRACELLULAR SPACE; MAGNOCELLULAR NUCLEUS; MALE; MAMMAL; NERVE CELL; NERVE ENDING; NEUROHYPOPHYSIS; NONHUMAN; PARACRINE SIGNALING; PERIKARYON; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; RNA TRANSLATION; SECRETORY GRANULE; TARGET CELL; ANIMAL; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; METABOLISM; PROCEDURES; SECRETORY VESICLE; SPRAGUE DAWLEY RAT; SUPRAOPTIC NUCLEUS; ULTRASTRUCTURE;

ANIMALS; GALANIN; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SECRETORY VESICLES; SUPRAOPTIC NUCLEUS; VASOPRESSINS;

EID: 0037325468     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02472.x     Document Type: Article

References (66)

1. Alonso, G., Bloch, B., Lutz-Bucher, B. & Assenmacher, I. (1981) Light- and electron-microscope differentiation of axons containing vasopressin and oxytocin in neurohypophyseal lobe of the rat. Neurosci. Lett., 25, 113-118.
2. Arvan, P. & Castle, D. (1992) Protein sorting and secretion granule formation in regulated secretory cells. Trends Cell. Biol., 2, 327-331.
3. Arvan, P. & Castle, D. (1998) Sorting and storage during secretory granules biogenesis: looking backward and looking forward. Biochem. J., 332, 593-610.
4. Bean, A.J., Zhang, X. & Hökfelt, T. (1994) Peptide secretion: What do we know? FASEB. J., 8, 630-638.
5. Bem-Barak, Y., Russell J.T., Whimall, M.H., Ozato, K. & Gainer, H. (1985) Neurophysin in the hypothalamo-neuropophyseal. I. Production and Characterization of monoclonal antibodies. J. Neurosci., 5, 81-97.
6. Bendayan, M. (1982) Double immunocytochemical labeling applying the protein A-gold technique. J. Histochem. Cytochem., 30, 81-85.
7. Bloch, B., Guitteny, A.F., Normand, E. & Chouham, S. (1990) Presence of neuropeptide messenger RNAs in neuronal processes. Neurosc. Lett., 109, 259-264.
8. Bondy, C.A., Whitnall, M.H., Brady, L.S. & Gainer, H. (1989) Coexisting peptides in hypothalamic neuroendocrine systems: some functional implications. Cell. Mol. Neurobiol., 9, 427-446.
9. Brownstein, M.J. & Mezey, E. (1986) Multiple chemical messengers in hypothalamic magnocellular neurons. Prog. Brain. Res., 68, 161-168.
10. Chun, J.Y., Korner, J., Kreiner, T., Scheller, R.H. & Axel, R. (1994) The function and differential sorting of a family of Aplysia prohormone processing enzymes. Neuron, 12, 831-844.
11. Dayanithi, G., Sabatier, N. & Widmer, H. (2000) Intracellular calcium signalling in magnocellular neurones of the rat supraoptic nucleus: understanding the autoregulatory mechanisms. Exp. Physiol., 85, 75S-84S.
12. Echard, A., Jollivet, F., Martinez, O., Lacapère, J., Rousselet, A., Janoueix-Lerosey, I. & Goud, B. (1998) Interaction of a Golgi-associated kinesin-like protein with Rab6. Science, 279, 580-585.
13. Elde, R., Hökfelt, T., Johansson, O., Ljungdhal, Å., Nilsson, G. & Jeffcoate, S.L. (1978) Immunohistochemical localization of peptides in the nervous system. In Hughes, J. (Ed.), Centrally Acting Peptides. Macmillan Press, London, pp. 17-36.
14. Fisher, J.M., Sossin, W., Newcomb, R. & Scheller, R.H. (1988) Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell, 54, 813-822.
15. Foletti, D.L., Prekeris, R. & Scheller, R.H. (1999) Generation and maintenance of neuronal polarity: mechanisms of transport and targeting. Neuron, 23, 641-644.
16. Fumagalli, G. & Zanini, A. (1985) In cow anterior pituitary, growth hormone and prolactin can be packed into separate granules of the same cell. J. Cell Biol., 100, 2019-2024.
17. Glombik, M.M. & Gerdes, H.H. (2000) Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie, 82, 315-326.
18. Gorr, S.U., Jain, R.K., Kuehn, U., Joyce, P.B.M. & Cowley, D.J. (2001) Comparative sorting of neuroendocrine secretory proteins: a search for common ground in a mosaic of sorting models and mechanisms. Mol. Cell. Endocrinol., 172, 1-6.
19. Hashimoto, S., Fumagalli, G., Zanini, A. & Meldolesi, J. (1987) Sorting of three secretory proteins to distinct secretory granules in acidophilic cells of cow anterior pituitary. J. Cell Biol., 105, 1579-1586.
20. Hekimi, S., Fischer-Lougheed, J. & O'Shea, M. (1991) Regulation of neuropeptide stoichiometry in neurosecretory cells. J. Neurosci., 11, 3246-3256.
21. Hirokawa, N. (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science, 279, 519-526.
22. Hökfelt, T. (1991) Neuropeptides in perspective: the last ten years. Neuron, 7, 867-879.
23. Hökfelt, T., Broberger, C., Xu, Z.Q., Sergeyev, V., Ubink, R. & Diez, M. (2000) Neuropeptides: an overview. Neuropharmacology, 39, 1337-1356.
24. Huang, X.F. & Arvan, P. (1994) Formation of insulin-containing secretory granules occurs within immature β-granules. J. Biol. Chem., 210, 20838-20844.
25. Ivell, R. & Richter, D. (1984) Structure and comparison of the oxytocin and vasopresin genes from rat. Proc. Natl Acad. Sci. USA, 81, 2006-2010.
26. Jamieson, J.D. & Palade, G.E. (1971) Synthesis, intracellular transport, and discharge of secretory proteins in stimulated pancreatic exocrine cells. J. Cell Biol., 50, 135-158.
27. Jung, L.J. & Scheller, R.H. (1991) Peptide processing and targeting in the neuronal secretory pathway. Science, 251, 1330-1335.
28. Kaplan, L.M., Spindel, E.R., Isselbacher, K.J. & Chin, W.W. (1988) Tissue-specific expression of the rat galanin gene. Proc. Natl Acad. Sci. USA, 85, 1065-1069.
29. Karhunen, T., Vilim, F.S., Alexeeva, V., Weiss, K.R. & Church, P.J. (2001) Targeting of peptidergic vesicles in cotransmitting terminals. J. Neurosci., 21, RC127(1-5).
30. Kelly, R.B. (1985) Pathways of protein secretion in eukaryotes. Science, 230, 25-32.
31. Klumperman, J., Spijker, S., van Minnen, J., Sharp-Baker, H., Smit, A.B. & Geraerts, W.P.M. (1996) Cell type-specific sorting of neuropeptides: a mechanism to modulate peptide composition of large dense-core vesicles. J. Neurosci., 16, 7930-7940.
32. Kuliawat, R., Prabakaran, D. & Arvan, P. (2000) Proinsulin endoproteolysis confers enhanced targeting of processed insulin to the regulated secretory pathway. Mol. Biol. Cell., 11, 1959-1972.
33. Landry, M., Åman, K. & Hökfelt, T. (1998) Galanin-R1 receptor in anterior and mid-hypothalamus: distribution and regulation. J. Comp. Neurol., 399, 321-340.
34. Landry, M. & Hökfelt, T. (1998) Subcellular localization of preprogalanin messenger RNA in perikarya and axons of hypothalamo-posthypophyseal magnocellular neurons: an in situ hybridization study. Neuroscience, 54, 897-912.
35. Landry, M., Holmberg, K., Zhang, X. & Hökfelt, T. (2000a) Effect of axotomy on expression of NPY, galanin, and NPY Y1 and Y2 receptors in dorsal root ganglia and the superior cervical ganglion studied with double-labeling in situ hybridization and immunohistochemistry. Exp. Neurol., 162, 361-384.
36. Landry, M., Roche, D. & Calas, A. (1995) Short-term effects of centrally administered galanin on the hyperosmotic stimulated expression of vasopressin in the rat hypothalamus: an in situ hybridization and immunohistochemistry study. Neuroendocrinology, 61, 393-404.
37. Landry, M., Roche, D., Vila-Porcile, E. & Calas, A. (2000b) Effects of centrally administered galanin (1-16) on galanin expression in the rat hypothalamus. Peptides, 21, 1725-1733.
38. Ludwig, M. (1998) Dendritic release of vasopressin and oxytocin. J. Neuroendocrinol., 10, 881-895.
39. Ludwig, M., Sabatier, N., Bull., P.M., Landgraf, R., Dayanithi, G. & Leng, G. (2002) Intracellular calcium stores regulate activity-dependant neuropeptide release from dendrites. Nature, 418, 85-89.
40. Martin, K.C., Casadio, A., Zhu, H.E.Y., Rose, J.C., Cen, M., Bailey, C.H. & Kandel, E.R. (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.
41. Meister, B., Cortès, R., Villar, M.J., Schalling, M. & Hökfelt, T. (1990) Peptides and transmitter enzymes in hypothalamic magnocellular neurons after administration of hyperosmotic stimuli: comparison between messenger RNA and peptide/protein levels. Cell Tissue Res., 260, 279-297.
42. Merighi, A. (2002) Costorage and coexistence of neuropeptides in the mammalian CNS. Prog. Neurobiol., 66, 161-190.
43. Merighi, A., Polak, J.M., Gibson, S.J., Gulbenkian, S., Valentino, K.L. & Peirone, S.M. (1988) Ultrastructural studies on calcitonin gene related peptide-, tachykinins- and somatostatin-immunoreactive neurons in rat dorsal root ganglia: evidence for the colocalization of different peptides in single secretory granules. Cell Tiss. Res., 254, 101-109.
44. Mohr, E. & Richter, D. (1992) Diversity of mRNAs in the axonal compartment of peptidergic neurons in the rat. Eur. J. Neurosci., 4, 870-876.
45. Morris, J.F., Budd, T.C., Epton, M.J., Ma, D., Pow, D.V. & Wang, H. (1998) Functions of the perikaryon and dendrites in magnocellular vasopressin-secreting neurons: new insights from ultrastructural studies. Prog. Brain Res., 119, 21-30.
46. Morris, J.F., Pow, D.V., Sokol, H.W. & Ward, A. (1993) Dendritic release of peptides from magnocellular neurons in normal rats, Brattleboro rats and mice with hereditary nephrogenic diabetes insipidus. In Gross, P., Richter, D. & Robertson, G.L. (Eds), Vasopressin. John Libbey Eurotext, Paris, pp. 171-182.
47. Muniz, M., Morsomme, P. & Riezman, H. (2001) Protein sorting upon exit from the endoplasmic reticulum. Cell, 104, 313-320.
48. Ozawa, H., Picart, R., Barret, A. & Tougard, C. (1994) Heterogeneity in the pattern of distribution of the specific hormonal product and secretogranins within the secretory granules of rat prolactin cells. J. Histochem. Cytochem., 42, 1097-1107.
49. Papas, S. & Bourque, C.W. (1998) Galanin inhibits continuous and phasic firing in rat hypothalamic magnocellular neurosecretory cells. J. Neurosci., 17, 6048-6056.
50. Pieribone, V.A., Xu, Z.Q., Zhang, X., Grillner, S., Bartfai, T. & Hökfelt, T. (1995) Galanin induces a hyperpolarization of norepinephrine-containing locus coeruleus neurons in the brainstem slice. Neuroscience, 64, 861-874.
51. Pow, D.V. & Morris, J.F. (1989) Dendrites of hypothalamic magnocellular neurons release neurohypophyseal peptides by exocytosis. Neuroscience, 32, 435-439.
52. Sawchenko, P.E. & Pfeiffer, S.W. (1988) Ultrastructural localization of neuropeptide Y and galanin immunoreactivity in the paraventricular nucleus of the hypothalamus in the rat. Brain Res., 47, 231-245.
53. Seidah, N.G. & Chretien, M. (1997) Eukaryotic protein processing: endoproteolysis of precursor proteins. Curr. Opin. Biotechnol., 8, 602-607.
54. Seybold, V., Elde, R. & Hökfelt, T. (1981) Terminals of reserpine-sensitive vasopressin-neurophysin neurons in the external layer of the rat median eminence. Endocrinology, 108, 1803-1809.
55. Shennan, K.I.J. (1996) Intracellular targeting of secretory proteins in neuroendocrine cells. Biochem. Soc. Trans., 24, 535-539.
56. Sossin, W.S., Fischer, J.M. & Scheller, R.H. (1990a) Sorting within the regulated secretory pathway occurs in the trans-Golgi network. J. Cell Biol., 110, 1-12.
57. Sossin, W.S. & Scheller, R.H. (1991) Biosynthesis and sorting of neuropeptides. Curr. Opin. Neurobiol., 1, 79-83.
58. Sossin, W.S., Sweet-Cordero, A. & Scheller, R.H. (1990b) Dale's hypotheis revisited: differential neuropeptides derived from a common precursor are targeted to different processes. Proc. Natl Acad. Sci. USA, 87, 4845-4848.
59. Tooze, S.A. (1998) Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochem. Biophys. Acta, 1404, 231-244.
60. Trembleau, A., Morales, M. & Bloom, F.E. (1994) 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, 39-53.
61. Van Leeuwen, F.W. (1992) Mutant vasopressin precursor producing cells of the homozygous Brattleboro rat as a model for co-expression of neuropeptides. Prog. Brain Res., 92, 149-155.
62. Vila-Porcile, E. & Barret, A. (1996) Structural and functional differences between prolactin cells from the inner and outer zones of the male rat anterior pituitary. Cell Tissue Res., 284, 247-259.
63. Wang, H., Ward, A.R. & Morris, J.F. (1995) Oestradiol acutely stimulates exocytosis of oxytocin and magnocellular neurons. Neuroscience, 68, 1179-1188.
64. Xu, Z.Q., Shi, T.J. & Hökfelt, T. (1997) Galanin/GMAP- and NPY-like immunoreactivty in locus coeruleus and noradrenergic nerve terminals in the hippocampal formation and cortex with notes on the galanin-R1 and -R2 receptors. J. Comp. Neurol., 392, 227-251.
65. Zhang, X., Nicholas, P. & Hökfelt, T. (1993) Ultrastructural studies on peptides in the dorsal horn of the spinal cord-I. Co-existence of galanin with other peptides in primary afferents in normal rats. Neuroscience, 57, 365-384.
66. Zhou, A., Webb, G., Zhu, X. & Steiner, D.F. (1999) Proteolytic processing in the secretory pathway. J. Biol. Chem., 274, 20745-20748.