Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1991 May;10(5):1275–1284. doi: 10.1002/j.1460-2075.1991.tb08069.x

GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion.

A Reetz 1, M Solimena 1, M Matteoli 1, F Folli 1, K Takei 1, P De Camilli 1
PMCID: PMC452782  PMID: 2022191

Abstract

GABA, a major inhibitory neurotransmitter of the brain, is also present at high concentration in pancreatic islets. Current evidence suggests that within islets GABA is secreted from beta-cells and regulates the function of mantle cells (alpha- and delta-cells). In the nervous system GABA is stored in, and secreted from, synaptic vesicles. The mechanism of GABA secretion from beta-cells remains to be elucidated. Recently the existence of synaptic-like microvesicles has been demonstrated in some peptide-secreting endocrine cells. The function of these vesicles is so far unknown. The proposed paracrine action of GABA in pancreatic islets makes beta-cells a useful model system to explore the possibility that synaptic-like microvesicles, like synaptic vesicles, are involved in the storage and release of non-peptide neurotransmitters. We report here the presence of synaptic-like microvesicles in beta-cells and in beta-cells. Some beta-cells in culture were found to extend neurite-like processes. When these were present, synaptic-like microvesicles were particularly concentrated in their distal portions. The GABA synthesizing enzyme, glutamic acid decarboxylase (GAD), was found to be localized around synaptic-like microvesicles. This was similar to the localization of GAD around synaptic vesicles in GABA-secreting neurons. GABA immunoreactivity was found to be concentrated in regions of beta-cells which were enriched in synaptic-like microvesicles. These findings suggest that in beta-cells synaptic-like microvesicles are storage organelles for GABA and support the hypothesis that storage of non-peptide signal molecules destined for secretion might be a general feature of synaptic-like microvesicles of endocrine cells.

Full text

PDF
1277

Images in this article

Selected References

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

  1. Alpert S., Hanahan D., Teitelman G. Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons. Cell. 1988 Apr 22;53(2):295–308. doi: 10.1016/0092-8674(88)90391-1. [DOI] [PubMed] [Google Scholar]
  2. Baekkeskov S., Aanstoot H. J., Christgau S., Reetz A., Solimena M., Cascalho M., Folli F., Richter-Olesen H., De Camilli P., Camilli P. D. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature. 1990 Sep 13;347(6289):151–156. doi: 10.1038/347151a0. [DOI] [PubMed] [Google Scholar]
  3. Banker G. A., Cowan W. M. Rat hippocampal neurons in dispersed cell culture. Brain Res. 1977 May 13;126(3):397–342. doi: 10.1016/0006-8993(77)90594-7. [DOI] [PubMed] [Google Scholar]
  4. Bartlett W. P., Banker G. A. An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts. J Neurosci. 1984 Aug;4(8):1944–1953. doi: 10.1523/JNEUROSCI.04-08-01944.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baumert M., Maycox P. R., Navone F., De Camilli P., Jahn R. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 1989 Feb;8(2):379–384. doi: 10.1002/j.1460-2075.1989.tb03388.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baumert M., Takei K., Hartinger J., Burger P. M., Fischer von Mollard G., Maycox P. R., De Camilli P., Jahn R. P29: a novel tyrosine-phosphorylated membrane protein present in small clear vesicles of neurons and endocrine cells. J Cell Biol. 1990 Apr;110(4):1285–1294. doi: 10.1083/jcb.110.4.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benedum U. M., Lamouroux A., Konecki D. S., Rosa P., Hille A., Baeuerle P. A., Frank R., Lottspeich F., Mallet J., Huttner W. B. The primary structure of human secretogranin I (chromogranin B): comparison with chromogranin A reveals homologous terminal domains and a large intervening variable region. EMBO J. 1987 May;6(5):1203–1211. doi: 10.1002/j.1460-2075.1987.tb02355.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bhathena S. J., Oie H. K., Gazdar A. F., Voyles N. R., Wilkins S. D., Recant L. Insulin, glucagon, and somatostatin receptors on cultured cells and clones from rat islet cell tumor. Diabetes. 1982 Jun;31(6 Pt 1):521–531. doi: 10.2337/diab.31.6.521. [DOI] [PubMed] [Google Scholar]
  9. Bonner-Weir S., Orci L. New perspectives on the microvasculature of the islets of Langerhans in the rat. Diabetes. 1982 Oct;31(10):883–889. doi: 10.2337/diab.31.10.883. [DOI] [PubMed] [Google Scholar]
  10. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem. 1981 Feb 25;256(4):1604–1607. [PubMed] [Google Scholar]
  11. Bowen K. M., Andrus L., Lafferty K. J. Successful allotransplantation of mouse pancreatic islets to nonimmunosuppressed recipients. Diabetes. 1980;29 (Suppl 1):98–104. doi: 10.2337/diab.29.1.s98. [DOI] [PubMed] [Google Scholar]
  12. Briel G., Gylfe E., Hellman B., Neuhoff V. Microdetermination of free amino acids in pancreatic islets isolated from obese-hyperglycemic mice. Acta Physiol Scand. 1972 Feb;84(2):247–253. doi: 10.1111/j.1748-1716.1972.tb05175.x. [DOI] [PubMed] [Google Scholar]
  13. Buckley K., Kelly R. B. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol. 1985 Apr;100(4):1284–1294. doi: 10.1083/jcb.100.4.1284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Burger P. M., Mehl E., Cameron P. L., Maycox P. R., Baumert M., Lottspeich F., De Camilli P., Jahn R. Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate. Neuron. 1989 Dec;3(6):715–720. doi: 10.1016/0896-6273(89)90240-7. [DOI] [PubMed] [Google Scholar]
  15. Cavagnini F., Pinto M., Dubini A., Invitti C., Cappelletti G., Polli E. E. Effects of gamma aminobutyric acid (GABA) and muscimol on endocrine pancreatic function in man. Metabolism. 1982 Jan;31(1):73–77. [PubMed] [Google Scholar]
  16. Chang Y. C., Gottlieb D. I. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J Neurosci. 1988 Jun;8(6):2123–2130. doi: 10.1523/JNEUROSCI.08-06-02123.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Christie M. R., Pipeleers D. G., Lernmark A., Baekkeskov S. Cellular and subcellular localization of an Mr 64,000 protein autoantigen in insulin-dependent diabetes. J Biol Chem. 1990 Jan 5;265(1):376–381. [PubMed] [Google Scholar]
  18. Clift-O'Grady L., Linstedt A. D., Lowe A. W., Grote E., Kelly R. B. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J Cell Biol. 1990 May;110(5):1693–1703. doi: 10.1083/jcb.110.5.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Colman P. G., Campbell I. L., Kay T. W., Harrison L. C. 64,000-Mr autoantigen in type I diabetes. Evidence against its surface location on human islets. Diabetes. 1987 Dec;36(12):1432–1440. doi: 10.2337/diab.36.12.1432. [DOI] [PubMed] [Google Scholar]
  20. Cutler D. F., Cramer L. P. Sorting during transport to the surface of PC12 cells: divergence of synaptic vesicle and secretory granule proteins. J Cell Biol. 1990 Mar;110(3):721–730. doi: 10.1083/jcb.110.3.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. De Camilli P., Harris S. M., Jr, Huttner W. B., Greengard P. Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J Cell Biol. 1983 May;96(5):1355–1373. doi: 10.1083/jcb.96.5.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Efrat S., Linde S., Kofod H., Spector D., Delannoy M., Grant S., Hanahan D., Baekkeskov S. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9037–9041. doi: 10.1073/pnas.85.23.9037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Eisenbarth G. S., Shimizu K., Bowring M. A., Wells S. Expression of receptors for tetanus toxin and monoclonal antibody A2B5 by pancreatic islet cells. Proc Natl Acad Sci U S A. 1982 Aug;79(16):5066–5070. doi: 10.1073/pnas.79.16.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Erdö S. L., Wolff J. R. gamma-Aminobutyric acid outside the mammalian brain. J Neurochem. 1990 Feb;54(2):363–372. doi: 10.1111/j.1471-4159.1990.tb01882.x. [DOI] [PubMed] [Google Scholar]
  26. Fischer von Mollard G., Mignery G. A., Baumert M., Perin M. S., Hanson T. J., Burger P. M., Jahn R., Südhof T. C. rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1988–1992. doi: 10.1073/pnas.87.5.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Garry D. J., Sorenson R. L., Coulter H. D. Ultrastructural localization of gamma amino butyric acid immunoreactivity in B cells of the rat pancreas. Diabetologia. 1987 Feb;30(2):115–119. doi: 10.1007/BF00274582. [DOI] [PubMed] [Google Scholar]
  28. Gazdar A. F., Chick W. L., Oie H. K., Sims H. L., King D. L., Weir G. C., Lauris V. Continuous, clonal, insulin- and somatostatin-secreting cell lines established from a transplantable rat islet cell tumor. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3519–3523. doi: 10.1073/pnas.77.6.3519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Goslin K., Banker G. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol. 1989 Apr;108(4):1507–1516. doi: 10.1083/jcb.108.4.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Halban P. A., Powers S. L., George K. L., Bonner-Weir S. Altered differentiated cell surface properties of transformed (RINm5F) compared with native adult rat pancreatic B cells. Endocrinology. 1988 Jul;123(1):113–119. doi: 10.1210/endo-123-1-113. [DOI] [PubMed] [Google Scholar]
  31. Hell J. W., Maycox P. R., Stadler H., Jahn R. Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J. 1988 Oct;7(10):3023–3029. doi: 10.1002/j.1460-2075.1988.tb03166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hökfelt T., Johansson O., Goldstein M. Chemical anatomy of the brain. Science. 1984 Sep 21;225(4668):1326–1334. doi: 10.1126/science.6147896. [DOI] [PubMed] [Google Scholar]
  33. Jahn R., Schiebler W., Ouimet C., Greengard P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4137–4141. doi: 10.1073/pnas.82.12.4137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Johnston P. A., Cameron P. L., Stukenbrok H., Jahn R., De Camilli P., Südhof T. C. Synaptophysin is targeted to similar microvesicles in CHO and PC12 cells. EMBO J. 1989 Oct;8(10):2863–2872. doi: 10.1002/j.1460-2075.1989.tb08434.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Julien J. F., Samama P., Mallet J. Rat brain glutamic acid decarboxylase sequence deduced from a cloned cDNA. J Neurochem. 1990 Feb;54(2):703–705. doi: 10.1111/j.1471-4159.1990.tb01928.x. [DOI] [PubMed] [Google Scholar]
  36. Katarova Z., Szabo G., Mugnaini E., Greenspan R. J. Molecular Identification of the 62 kd Form of Glutamic Acid Decarboxylase from the Mouse. Eur J Neurosci. 1990;2(3):190–202. doi: 10.1111/j.1460-9568.1990.tb00412.x. [DOI] [PubMed] [Google Scholar]
  37. Kobayashi Y., Kaufman D. L., Tobin A. J. Glutamic acid decarboxylase cDNA: nucleotide sequence encoding an enzymatically active fusion protein. J Neurosci. 1987 Sep;7(9):2768–2772. doi: 10.1523/JNEUROSCI.07-09-02768.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  39. Le Douarin N. M. On the origin of pancreatic endocrine cells. Cell. 1988 Apr 22;53(2):169–171. doi: 10.1016/0092-8674(88)90375-3. [DOI] [PubMed] [Google Scholar]
  40. Legay F., Henry S., Tappaz M. Evidence for two distinct forms of native glutamic acid decarboxylase in rat brain soluble extract: an immunoblotting study. J Neurochem. 1987 Apr;48(4):1022–1026. doi: 10.1111/j.1471-4159.1987.tb05620.x. [DOI] [PubMed] [Google Scholar]
  41. Matthew W. D., Tsavaler L., Reichardt L. F. Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol. 1981 Oct;91(1):257–269. doi: 10.1083/jcb.91.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. McLaughlin B. J., Wood J. G., Saito K., Roberts E., Wu J. Y. The fine structural localization of glutamate decarboxylase in developing axonal processes and presynaptic terminals of rodent cerebellum. Brain Res. 1975 Mar 7;85(3):355–371. doi: 10.1016/0006-8993(75)90813-6. [DOI] [PubMed] [Google Scholar]
  43. Mignery G. A., Südhof T. C., Takei K., De Camilli P. Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature. 1989 Nov 9;342(6246):192–195. doi: 10.1038/342192a0. [DOI] [PubMed] [Google Scholar]
  44. Navone F., Di Gioia G., Jahn R., Browning M., Greengard P., De Camilli P. Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J Cell Biol. 1989 Dec;109(6 Pt 2):3425–3433. doi: 10.1083/jcb.109.6.3425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Navone F., Jahn R., Di Gioia G., Stukenbrok H., Greengard P., De Camilli P. Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol. 1986 Dec;103(6 Pt 1):2511–2527. doi: 10.1083/jcb.103.6.2511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Oertel W. H., Schmechel D. E., Mugnaini E., Tappaz M. L., Kopin I. J. Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience. 1981;6(12):2715–2735. doi: 10.1016/0306-4522(81)90115-9. [DOI] [PubMed] [Google Scholar]
  47. Oertel W. H., Schmechel D. E., Tappaz M. L., Kopin I. J. Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience. 1981;6(12):2689–2700. doi: 10.1016/0306-4522(81)90113-5. [DOI] [PubMed] [Google Scholar]
  48. Okada Y., Taniguchi H., Schimada C. High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma. Science. 1976 Nov 5;194(4265):620–622. doi: 10.1126/science.185693. [DOI] [PubMed] [Google Scholar]
  49. Passariello N., Giugliano D., Torella R., Sgambato S., Coppola L., Frascolla N. A possible role of gamma-aminobutyric acid in the control of the endocrine pancreas. J Clin Endocrinol Metab. 1982 Jun;54(6):1145–1149. doi: 10.1210/jcem-54-6-1145. [DOI] [PubMed] [Google Scholar]
  50. Pearse A. G. The diffuse neuroendocrine system and the apud concept: related "endocrine" peptides in brain, intestine, pituitary, placenta, and anuran cutaneous glands. Med Biol. 1977 Jun;55(3):115–125. [PubMed] [Google Scholar]
  51. Powers A. C., Efrat S., Mojsov S., Spector D., Habener J. F., Hanahan D. Proglucagon processing similar to normal islets in pancreatic alpha-like cell line derived from transgenic mouse tumor. Diabetes. 1990 Apr;39(4):406–414. doi: 10.2337/diab.39.4.406. [DOI] [PubMed] [Google Scholar]
  52. Robbins M. S., Grouse L. H., Sorenson R. L., Elde R. P. Effect of muscimol on glucose-stimulated somatostatin and insulin release from the isolated, perfused rat pancreas. Diabetes. 1981 Feb;30(2):168–171. doi: 10.2337/diab.30.2.168. [DOI] [PubMed] [Google Scholar]
  53. Rorsman P., Berggren P. O., Bokvist K., Ericson H., Möhler H., Ostenson C. G., Smith P. A. Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels. Nature. 1989 Sep 21;341(6239):233–236. doi: 10.1038/341233a0. [DOI] [PubMed] [Google Scholar]
  54. Rosa P., Fumagalli G., Zanini A., Huttner W. B. The major tyrosine-sulfated protein of the bovine anterior pituitary is a secretory protein present in gonadotrophs, thyrotrophs, mammotrophs, and corticotrophs. J Cell Biol. 1985 Mar;100(3):928–937. doi: 10.1083/jcb.100.3.928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rosa P., Hille A., Lee R. W., Zanini A., De Camilli P., Huttner W. B. Secretogranins I and II: two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway. J Cell Biol. 1985 Nov;101(5 Pt 1):1999–2011. doi: 10.1083/jcb.101.5.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Saito K., Barber R., Wu J., Matsuda T., Roberts E., Vaughn J. E. Immunohistochemical localization of glutamate decarboxylase in rat cerebellum. Proc Natl Acad Sci U S A. 1974 Feb;71(2):269–273. doi: 10.1073/pnas.71.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schwartz E. A. Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science. 1987 Oct 16;238(4825):350–355. doi: 10.1126/science.2443977. [DOI] [PubMed] [Google Scholar]
  58. Schweitzer E. S., Paddock S. Localization of human growth hormone to a sub-set of cytoplasmic vesicles in transfected PC12 cells. J Cell Sci. 1990 Jul;96(Pt 3):375–381. doi: 10.1242/jcs.96.3.375. [DOI] [PubMed] [Google Scholar]
  59. Solimena M., Folli F., Aparisi R., Pozza G., De Camilli P. Autoantibodies to GABA-ergic neurons and pancreatic beta cells in stiff-man syndrome. N Engl J Med. 1990 May 31;322(22):1555–1560. doi: 10.1056/NEJM199005313222202. [DOI] [PubMed] [Google Scholar]
  60. Storm-Mathisen J., Leknes A. K., Bore A. T., Vaaland J. L., Edminson P., Haug F. M., Ottersen O. P. First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature. 1983 Feb 10;301(5900):517–520. doi: 10.1038/301517a0. [DOI] [PubMed] [Google Scholar]
  61. Teitelman G., Lee J. K., Alpert S. Expression of cell type-specific markers during pancreatic development in the mouse: implications for pancreatic cell lineages. Cell Tissue Res. 1987 Nov;250(2):435–439. doi: 10.1007/BF00219089. [DOI] [PubMed] [Google Scholar]
  62. Teitelman G., Lee J. K. Cell lineage analysis of pancreatic islet development: glucagon and insulin cells arise from catecholaminergic precursors present in the pancreatic duct. Dev Biol. 1987 Jun;121(2):454–466. doi: 10.1016/0012-1606(87)90182-5. [DOI] [PubMed] [Google Scholar]
  63. Tooze J., Burke B. Accumulation of adrenocorticotropin secretory granules in the midbody of telophase AtT20 cells: evidence that secretory granules move anterogradely along microtubules. J Cell Biol. 1987 Apr;104(4):1047–1057. doi: 10.1083/jcb.104.4.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Tooze J., Hollinshead M., Fuller S. D., Tooze S. A., Huttner W. B. Morphological and biochemical evidence showing neuronal properties in AtT-20 cells and their growth cones. Eur J Cell Biol. 1989 Aug;49(2):259–273. [PubMed] [Google Scholar]
  65. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Vincent S. R., Hökfelt T., Wu J. Y., Elde R. P., Morgan L. M., Kimmel J. R. Immunohistochemical studies of the GABA system in the pancreas. Neuroendocrinology. 1983;36(3):197–204. doi: 10.1159/000123456. [DOI] [PubMed] [Google Scholar]
  67. Wenthold R. J., Zempel J. M., Parakkal M. H., Reeks K. A., Altschuler R. A. Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Res. 1986 Aug 13;380(1):7–18. doi: 10.1016/0006-8993(86)91423-x. [DOI] [PubMed] [Google Scholar]
  68. 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]
  69. Wiedenmann B., Rehm H., Knierim M., Becker C. M. Fractionation of synaptophysin-containing vesicles from rat brain and cultured PC12 pheochromocytoma cells. FEBS Lett. 1988 Nov 21;240(1-2):71–77. doi: 10.1016/0014-5793(88)80342-9. [DOI] [PubMed] [Google Scholar]
  70. Wyborski R. J., Bond R. W., Gottlieb D. I. Characterization of a cDNA coding for rat glutamic acid decarboxylase. Brain Res Mol Brain Res. 1990 Aug;8(3):193–198. doi: 10.1016/0169-328x(90)90016-7. [DOI] [PubMed] [Google Scholar]
  71. Yuan L., Barriocanal J. G., Bonifacino J. S., Sandoval I. V. Two integral membrane proteins located in the cis-middle and trans-part of the Golgi system acquire sialylated N-linked carbohydrates and display different turnovers and sensitivity to cAMP-dependent phosphorylation. J Cell Biol. 1987 Jul;105(1):215–227. doi: 10.1083/jcb.105.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. 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 The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES