Skip to main content
NCBI home page
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 Aug 1;92(16):7342–7346. doi: 10.1073/pnas.92.16.7342

Neurosecretory vesicles can be hybrids of synaptic vesicles and secretory granules.

R Bauerfeind 1, R Jelinek 1, A Hellwig 1, W B Huttner 1
PMCID: PMC41335  PMID: 7638193

Abstract

We have investigated the relationship of the so-called small dense core vesicle (SDCV), the major catecholamine-containing neurosecretory vesicle of sympathetic neurons, to synaptic vesicles containing classic neurotransmitters and secretory granules containing neuropeptides. SDCVs contain membrane proteins characteristic of synaptic vesicles such as synaptophysin and synaptoporin. However, SDCVs also contain membrane proteins characteristic of certain secretory granules like the vesicular monoamine transporter and the membrane-bound form of dopamine beta-hydroxylase. In neurites of sympathetic neurons, synaptophysin and dopamine beta-hydroxylase are found in distinct vesicles, consistent with their transport from the trans-Golgi network to the site of SDCV formation in constitutive secretory vesicles and secretory granules, respectively. Hence, SDCVs constitute a distinct type of neurosecretory vesicle that is a hybrid of the synaptic vesicle and the secretory granule membranes and that originates from the contribution of both the constitutive and the regulated pathway of protein secretion.

Full text

PDF
7342

Images in this article

7343Fig. 1
on p.7343
7345Fig. 3
on p.7345
7345Fig. 4
on p.7345

Selected References

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

  1. Annaert W. G., Quatacker J., Llona I., De Potter W. P. Differences in the distribution of cytochrome b561 and synaptophysin in dog splenic nerve: a biochemical and immunocytochemical study. J Neurochem. 1994 Jan;62(1):265–274. doi: 10.1046/j.1471-4159.1994.62010265.x. [DOI] [PubMed] [Google Scholar]
  2. Brose N., Petrenko A. G., Südhof T. C., Jahn R. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science. 1992 May 15;256(5059):1021–1025. doi: 10.1126/science.1589771. [DOI] [PubMed] [Google Scholar]
  3. Burgess T. L., Kelly R. B. Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987;3:243–293. doi: 10.1146/annurev.cb.03.110187.001331. [DOI] [PubMed] [Google Scholar]
  4. De Camilli P., Jahn R. Pathways to regulated exocytosis in neurons. Annu Rev Physiol. 1990;52:625–645. doi: 10.1146/annurev.ph.52.030190.003205. [DOI] [PubMed] [Google Scholar]
  5. Fried G., Lagercrantz H., Hökfelt T. Improved isolation of small noradrenergic vesicles from rat seminal ducts following castration. A density gradient centrifugation and morphological study. Neuroscience. 1978;3(12):1271–1291. doi: 10.1016/0306-4522(78)90147-1. [DOI] [PubMed] [Google Scholar]
  6. Griffiths G., McDowall A., Back R., Dubochet J. On the preparation of cryosections for immunocytochemistry. J Ultrastruct Res. 1984 Oct;89(1):65–78. doi: 10.1016/s0022-5320(84)80024-6. [DOI] [PubMed] [Google Scholar]
  7. Griffiths G., Simons K., Warren G., Tokuyasu K. T. Immunoelectron microscopy using thin, frozen sections: application to studies of the intracellular transport of Semliki Forest virus spike glycoproteins. Methods Enzymol. 1983;96:466–485. doi: 10.1016/s0076-6879(83)96041-x. [DOI] [PubMed] [Google Scholar]
  8. Gruenberg J., Howell K. E. Immuno-isolation of vesicles using antigenic sites either located on the cytoplasmic or the exoplasmic domain of an implanted viral protein. A quantitative analysis. Eur J Cell Biol. 1985 Sep;38(2):312–321. [PubMed] [Google Scholar]
  9. Johnson R. G., Jr Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol Rev. 1988 Jan;68(1):232–307. doi: 10.1152/physrev.1988.68.1.232. [DOI] [PubMed] [Google Scholar]
  10. Knaus P., Marquèze-Pouey B., Scherer H., Betz H. Synaptoporin, a novel putative channel protein of synaptic vesicles. Neuron. 1990 Oct;5(4):453–462. doi: 10.1016/0896-6273(90)90084-s. [DOI] [PubMed] [Google Scholar]
  11. Lowe A. W., Madeddu L., Kelly R. B. Endocrine secretory granules and neuronal synaptic vesicles have three integral membrane proteins in common. J Cell Biol. 1988 Jan;106(1):51–59. doi: 10.1083/jcb.106.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McMahon A., Geertman R., Sabban E. L. Rat dopamine beta-hydroxylase: molecular cloning and characterization of the cDNA and regulation of the mRNA by reserpine. J Neurosci Res. 1990 Mar;25(3):395–404. doi: 10.1002/jnr.490250317. [DOI] [PubMed] [Google Scholar]
  13. Neuman B., Wiedermann C. J., Fischer-Colbrie R., Schober M., Sperk G., Winkler H. Biochemical and functional properties of large and small dense-core vesicles in sympathetic nerves of rat and ox vas deferens. Neuroscience. 1984 Nov;13(3):921–931. doi: 10.1016/0306-4522(84)90106-4. [DOI] [PubMed] [Google Scholar]
  14. Patzak A., Winkler H. Exocytotic exposure and recycling of membrane antigens of chromaffin granules: ultrastructural evaluation after immunolabeling. J Cell Biol. 1986 Feb;102(2):510–515. doi: 10.1083/jcb.102.2.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Rosa P., Bassetti M., Weiss U., Huttner W. B. Widespread occurrence of chromogranins/secretogranins in the matrix of secretory granules of endocrinologically silent pituitary adenomas. J Histochem Cytochem. 1992 Apr;40(4):523–533. doi: 10.1177/40.4.1552186. [DOI] [PubMed] [Google Scholar]
  16. Rosa P., Weiss U., Pepperkok R., Ansorge W., Niehrs C., Stelzer E. H., Huttner W. B. An antibody against secretogranin I (chromogranin B) is packaged into secretory granules. J Cell Biol. 1989 Jul;109(1):17–34. doi: 10.1083/jcb.109.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Régnier-Vigouroux A., Huttner W. B. Biogenesis of small synaptic vesicles and synaptic-like microvesicles. Neurochem Res. 1993 Jan;18(1):59–64. doi: 10.1007/BF00966923. [DOI] [PubMed] [Google Scholar]
  18. Schmidle T., Weiler R., Desnos C., Scherman D., Fischer-Colbrie R., Floor E., Winkler H. Synaptin/synaptophysin, p65 and SV2: their presence in adrenal chromaffin granules and sympathetic large dense core vesicles. Biochim Biophys Acta. 1991 Nov 7;1060(3):251–256. doi: 10.1016/s0005-2728(05)80314-7. [DOI] [PubMed] [Google Scholar]
  19. Schwarzenbrunner U., Schmidle T., Obendorf D., Scherman D., Hook V., Fischer-Colbrie R., Winkler H. Sympathetic axons and nerve terminals: the protein composition of small and large dense-core and of a third type of vesicles. Neuroscience. 1990;37(3):819–827. doi: 10.1016/0306-4522(90)90111-g. [DOI] [PubMed] [Google Scholar]
  20. Slot J. W., Geuze H. J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol. 1985 Jul;38(1):87–93. [PubMed] [Google Scholar]
  21. Smith A. D. Subcellular localisation of noradrenaline in sympathetic neurons. Pharmacol Rev. 1972 Sep;24(3):435–457. [PubMed] [Google Scholar]
  22. Taljanidisz J., Stewart L., Smith A. J., Klinman J. P. Structure of bovine adrenal dopamine beta-monooxygenase, as deduced from cDNA and protein sequencing: evidence that the membrane-bound form of the enzyme is anchored by an uncleaved signal peptide. Biochemistry. 1989 Dec 26;28(26):10054–10061. doi: 10.1021/bi00452a026. [DOI] [PubMed] [Google Scholar]
  23. Thureson-Klein A. K., Klein R. L. Exocytosis from neuronal large dense-cored vesicles. Int Rev Cytol. 1990;121:67–126. doi: 10.1016/s0074-7696(08)60659-2. [DOI] [PubMed] [Google Scholar]
  24. Wiedenmann B., Franke W. W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 1985 Jul;41(3):1017–1028. doi: 10.1016/s0092-8674(85)80082-9. [DOI] [PubMed] [Google Scholar]
  25. Winkler H., Sietzen M., Schober M. The life cycle of catecholamine-storing vesicles. Ann N Y Acad Sci. 1987;493:3–19. doi: 10.1111/j.1749-6632.1987.tb27176.x. [DOI] [PubMed] [Google Scholar]
  26. de Camilli P., Navone F. Regulated secretory pathways of neurons and their relation to the regulated secretory pathway of endocrine cells. Ann N Y Acad Sci. 1987;493:461–479. doi: 10.1111/j.1749-6632.1987.tb27231.x. [DOI] [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