Storage of GABA in chromaffin granules and not in synaptic-like microvesicles in rat adrenal medullary cells

Journal of Neurochemistry

Volumn 114, Issue 2, 2010, Pages 617-626

  Harada, Keita ^a   Matsuoka, Hidetada ^a   Nakamura, Jun ^a   Fukuda, Mitsunori ^b   Inoue, Masumi ^a  

^a UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

aminobutyric acid; chromaffin cell; chromaffin granules; GABA transporter; PC12; synaptic like microvesicles

Indexed keywords

ACETYLCHOLINE; GREEN FLUORESCENT PROTEIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ADRENAL MEDULLA; ANIMAL CELL; ARTICLE; CATECHOLAMINE RELEASE; CELLULAR DISTRIBUTION; CHROMAFFIN GRANULE; CONTROLLED STUDY; COW; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; MALE; NONHUMAN; PARACRINE SIGNALING; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; RAT; SUCROSE DENSITY GRADIENT CENTRIFUGATION; SYNAPSE VESICLE;

ADRENAL MEDULLA; ANIMALS; CATTLE; CELL FRACTIONATION; CHROMAFFIN GRANULES; GAMMA-AMINOBUTYRIC ACID; MALE; PC12 CELLS; RATS; RATS, WISTAR; SECRETORY VESICLES; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

BOVINAE; RATTUS;

EID: 77953851666     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06792.x     Document Type: Article

References (37)

1. Annaert W. G., Llona I., Backer A. C., Jacob W. A. De Potter W. P. (1993) Catecholamines are present in a synaptic-like microvesicle-enriched fraction from bovine adrenal medulla. J. Neurochem. 60, 1746 1754.
2. Bisby M. A. Fillenz M. (1971) The storage of endogenous noradrenaline in sympathetic nerve terminals. J. Physiol. (Lond.) 215, 163 179.
3. Burger P. M., Hell J., Mehl E., Krasel C., Lottspeich F. Jahn R. (1991) GABA and glycine in synaptic vesicles: storage and transport characteristics. Neuron 7, 287 293.
4. Chaudhry F. A., Edwards R. H. Fonnum F. (2008) Vesicular neurotransmitter transporters as targets for endogenous and exogenous toxic substances. Annu. Rev. Pharmacol. Toxicol. 48, 277 301.
5. Cutler D. F. Cramer L. P. (1990) Sorting during transport to the surface of PC12 cells: Divergence of synaptic vesicle and secretory granule proteins. J. Cell Biol. 110, 721 730.
6. Dumoulin A., Rostaing P., Bedet C., Lévi S., Isambert M.-F., Henry J.-P., Triller A. Gasnier B. (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J. Cell Sci. 112, 811 823.
7. Ferreira L. T., Santos M. S., Kolmakova N. G. et al. (2005) Structural requirements for steady-state localization of the vesicular acetylcholine transporter. J. Neurochem. 94, 957 969.
8. Gao Y. S., Alvarez C., Nelson D. S. Sztul E. (1998) Molecular cloning, characterization, and dynamics of rat formiminotransferase cyclodeaminase, a Golgi-associated 58-kDa protein. J. Biol. Chem. 273, 33825 33834.
9. Grabner C. P., Price S. D., Lysakowski A. Fox A. P. (2005) Mouse chromaffin cells have two populations of dense core vesicles. J. Neurophysiol. 94, 2093 2104.
10. Holz R. W. (1979) Measurement of membrane potential of chromaffin granules by the accumulation of triphenylmethylphosphonium cation. J. Biol. Chem. 254, 6703 6709.
11. Inoue M., Fujishiro N., Ogawa K., Muroi M., Sakamoto Y., Imanaga I. Shioda S. (2000) Pituitary adenylate cyclase-activating polypeptide may function as a neuromodulator in guinea-pig adrenal medulla. J. Physiol. (Lond.) 528, 473 487.
12. 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.
13. 2+-dependent exocytosis: implications of kinetic diversity for secretory function. Trends Neurosci. 22, 88 93.
14. Kim T., Gondré-Lewis M. C., Arnaoutova I. Loh Y. P. (2006) Dense-core secretory granule biogenesis. Physiology 21, 124 133.
15. A receptor is associated with the receptor subunit composition. J. Physiol. (Lond.) 492, 431 443.
16. Liu Y. Edwards R. H. (1997) Differential localization of vesicular acetylcholine and monoamine transporters in PC12 cells but not CHO cells. J. Cell Biol. 139, 907 916.
17. Maron R., Stern Y., Kanner B. I. Schuldiner S. (1983) Functional asymmetry of the amine transporter from chromaffin granules. J. Biol. Chem. 258, 11476 11481.
18. Matsuoka H., Harada K., Endo Y., Warashina A., Doi Y., Nakamura J. Inoue M. (2008) Molecular mechanisms supporting a paracrine role of GABA in rat adrenal medullary cells. J. Physiol. (Lond.) 586, 4825 4842.
19. Melkikh A. V. Seleznev V. D. (2007) Models of active transport of neurotransmitters in synaptic vesicles. J. Theor. Biol. 248, 350 353.
20. Montesinos M. S., Machado J. D., Camacho M. et al. (2008) The crucial role of chromogranins in storage and exocytosis revealed using chromaffin cells from chromogranin A null mouse. J. Neurosci. 28, 3350 3358.
21. Moriyama Y., Yamamoto A., Yamada H., Tashiro Y., Tomochika K., Takahashi M., Maeda M. Futai M. (1995) Microvesicles isolated from bovine posterior pituitary accumulate norepinephrine. J. Biol. Chem. 270, 11424 11429.
22. Nakamura N., Rabouille C., Watson R., Nilsson T., Hui N., Slusarewicz P., Kreis T. E. Warren G. (1995) Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131, 1715 1726.
23. Navone F., Jahn R., Di Gioia G., Stukenbrok H., Greengard P. De Camilli P. (1986) Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J. Cell Biol. 103, 2511 2527.
24. Navone F., Di Gioia G., Jahn R., Browning M., Greengard P. De Camilli P. (1989) Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J. Cell Biol. 109, 3425 3433.
25. Neuman B., Wiedermann C. J., Fischer-Colbrie R., Schober M., Sperk G. Winkler H. (1984) Biochemical and functional properties of large and small dense-core vesicles in sympathetic nerves of rat and ox vas deferens. Neuroscience 13, 921 931.
26. A receptors on bovine adrenomedullary chromaffin cells. Pflugers Arch. 415, 95 103.
27. Reetz A., Solimena M., Matteoli M., Foll F., Takei K. De Camilli P. (1991) GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J. 10, 1275 1284.
28. Rorsman P., Berggren P. O., Bokvist K., Ericson H., Möhler H., Östenson C. G. Smith P. A. (1989) Glucose-inhibition of glucagon secretion involves activation of GABA A-receptor chloride channels. Nature 341, 233 236.
29. Südhof T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509 547.
30. Tandon A., Bannykh S., Kowalchyk J. A., Banerjee A., Martin T. F. Balch W. E. (1998) Differential regulation of exocytosis by calcium and CAPS in semi-intact synaptosomes. Neuron 21, 147 154.
31. Thomas-Reetz A. C. De Camilli P. (1994) A role for synaptic vesicles in non-neuronal cells: clues from pancreatic β cells and from chromaffin cells. FASEB J. 8, 209 216.
32. Tooze S. A., Flatmark T., Tooze J. Huttner W. B. (1991) Characterization of the immature secretory granule biogenesis. J. Cell Biol. 115, 1491 1503.
33. Ungar A. Phillips J. H. (1983) Regulation of the adrenal medulla. Physiol. Rev. 63, 787 835.
34. Videen J. S., Mezger M. S., Chan Y.-M. O'Connor D. T. (1992) Calcium and catecholamine interactions with adrenal chromogranins. Comparison of driving forces in binding and aggregation. J. Biol. Chem. 267, 3066 3073.
35. Wendt A., Birnir B., Buschard K., Gromada J., Salehi A., Sewing S., Rorsman P. Braun M. (2004) Glucose inhibition of glucagon secretion from rat α-cells is mediated by GABA released from neighboring β-cells. Diabetes 53, 1038 1045.
36. Winkler H. Westhead E. (1980) The molecular organization of adrenal chromaffin granules. Neuroscience 5, 1803 1823.
37. Wojcik S. M., Katsurabayashi S., Guillemin I., Friauf E., Rosenmund C., Brose N. Rhee J. -S. (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50, 575 587.