Differential localization of vesicular acetylcholine and monoamine transporters in PC12 cells but not CHO cells

Journal of Cell Biology

Volumn 139, Issue 4, 1997, Pages 907-916

  Liu, Yongjian ^a   Edwards, Robert H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CARRIER PROTEIN; MONOAMINE; SYNAPTOPHYSIN;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL VACUOLE; CELLULAR DISTRIBUTION; CHO CELL; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL;

ACETYLCHOLINE; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL COMPARTMENTATION; CELL MEMBRANE; CHO CELLS; CRICETINAE; ENDOSOMES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; INTRACELLULAR MEMBRANES; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NEUROPEPTIDES; PC12 CELLS; PEPTIDES; RATS; RECEPTORS, TRANSFERRIN; SYNAPTIC VESICLES; SYNAPTOPHYSIN; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VESICULAR BIOGENIC AMINE TRANSPORT PROTEINS; VESICULAR TRANSPORT PROTEINS;

ANIMALIA;

EID: 0030709324     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.4.907     Document Type: Article

References (61)

1. Alfonso, A., K. Grundahl, J.S. Duerr, H.-P. Han, and J.B. Rand. 1993. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science. 261:617-619.
2. Anderson, D.C., S.C. King, and S.M. Parsons. 1982. Proton gradient linkage to active uptake of 3H-acetylcholine by Torpedo electric organ synaptic vesicles. Biochemistry. 21:3037-3043.
3. Bauerfeind, R., A. Regnier-Vigouroux, T. Flatmark, and W.B. Huttner. 1993. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron. 11:105-121.
4. Bejanin, S., R. Cervini, J. Mallet, and S. Berrard. 1994. A unique gene organization for two cholinergic markers, choline acetyltransferase and a putative vesicular transporter of acetylcholine. J. Biol. Chem. 269:21944-21947.
5. Blumberg, D., and E.S. Schweitzer. 1992. Vesamicol binding to subcellular membranes that are distinct from catecholaminergic vesicles in PC12 cells. J. Neurochem. 58:801-810.
6. Bonzelius, F., G.A. Herman, M.H. Cardone, K.E. Mostov, and R.B. Kelly. 1994. The polymeric immunoglobulin receptor accumulates in specialized endosomes but not synaptic vesicles within the neuntes of transfected neuroendocrine PC12 cells. J. Cell Biol. 127:1603-1616.
7. Calakos, N., and R.H. Scheller. 1996. Synaptic vesicle biogenesis, docking and fusion: a molecular description. Physiol. Rev. 76:1-29.
8. Cameron, P.L., T.C. Sudhof, R. Jahn, and P. de Camilli. 1991. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J. Cell Biol. 115:151-164.
9. Chavez, R.A., S.G. Miller, and H.-P. Moore. 1996. A biosynthetic regulated secretory pathway in constitutive secretory cells. J. Cell Biol. 133:1177-1191.
10. Chen, W.J., J.L. Goldstein, and M.S. Brown. 1990. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265:3116-3123.
11. Clift-O'Grady, L., A.D. Linstedt, A.W. Lowe, E. Grote, and R.B. Kelly. 1990. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC12. J. Cell Biol. 110:1693-1703.
12. Cosson, P., and F. Letourneur. 1994. Coatamer interaction with di-lysine endoplasmic reticulum retention motifs. Science. 263:1629-1631.
13. De Camilli, P., and R. Jahn. 1990. Pathways to regulated exocytosis in neurons. Annu. Rev. Physiol. 52:625-645.
14. Disdier, M., J.H. Morrissey, R.D. Fugate, D.F. Bainton, and R.P. McEver. 1992. Cytoplasmic domain of P-selectin (CD62) contains the signal for sorting into the regulated secretory pathway. Mol. Biol. Cell. 3:309-321.
15. Dittie, A.S., N. Hajibagheri, and S.A. Tooze. 1996. The AP-1 adaptor complex binds to immature secretory granules from PC12 cells and is regulated by ADP-ribosylation factor. J. Cell Biol. 132:523-536.
16. Edwards, R.H. 1992. The transport of neurotransmitters into synaptic vesicles. Curr. Opin. Neurobiol. 2:586-594.
17. Edwards, R.H. 1993. Neural degeneration and the transport of neurotransmitters. Annu. Neurol. 34:638-645.
18. Erickson, J.D., L.E. Eiden, and B.J. Hoffman. 1992. Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc. Natl. Acad. Sci. USA. 89:10993-10997.
19. Erickson, J.D., H. Varoqui, M.D. Schafer, W. Modi, M.F. Diebler, E. Weihe, J. Rand, L.E. Eiden, T.I. Bonner, and T.B. Usdin. 1994. Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J. Biol. Chem. 269:21929-21932.
20. Farquhar, M.G., J.J. Reid, and L.W. Daniell. 1978. Intracellular transport and packaging of prolactin: a quantitative electron microscope autoradiographic study of mamotrophs dissociated from rat pituitaries. Endocrinology. 102:296-311.
21. Gilmor, M.L., N.R. Nash, A. Roghani, R.H. Edwards, H. Yi, S.M. Hersch, and A.I. Levey. 1996. Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J. Neurosci. 16:2179-2190.
22. Greene, L.A., and A.S. Tischler. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA. 73:2424-2428.
23. Greene, L.A., and G. Rein. 1977. Synthesis, storage and release of acetylcholine by a noradrenergic pheochromocytoma cell line. Nature. 268: 349-351.
24. Hell, J.W., P.R. Maycox, and R. Jahn. 1990. Energy dependence and functional reconstitution of the γ-aminobutyric acid carrier from synaptic vesicles. J. Biol. Chem. 265:2111-2117.
25. Johnson, E.F., and S. Kornfeld. 1992. The cytoplasmic tail of the mannose-6-phosphate/insulin-like growth factor-II receptor has two signals for lysosomal enzyme sorting in the Golgi. J. Cell Biol. 119:249-257.
26. Johnson, R.G. 1988. Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol. Rev. 68:232-307.
27. Johnston, P.A., P.L. Cameron, H. Stukenbrok, R. Jahn, P. De Camilli, and T.C. Sudhof. 1989. Synaptophysin is targeted to similar microvesicles in CHO and PC12 cells. EMBO (Eur. Mol. Biol. Organ.) J. 8:2863-2872.
28. Kelly, R.B. 1991. Secretory granule and synaptic vesicle formation. Curr. Opin. Cell Biol. 3:654-660.
29. Kelly, R.B. 1993. Storage and release of neurotransmitters. Cell. 72:43-53.
30. Kish, P.E., C. Fischer-Bovenkerk, and T. Ueda. 1989. Active transport of γ-aminobutyric acid and glycine into synaptic vesicles. Proc. Natl. Acad. Sci. USA. 86:3877-3881.
31. Koedam, J.A., E.M. Cramer, E. Briend, B. Farie, and D.D. Wagner. 1992. P-selectin, a granule membrane protein of platelets and endothelial cells, follows the regulated secretory pathway in AtT20 cells. J. Cell Biol. 116: 617-625.
32. Kuliawat, R., and P. Arvan. 1992. Protein targeting via the "constitutive-like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule component. J. Cell Biol. 118:521-529.
33. Kuliawat, R., and P. Arvan. 1994. Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic β-cells. J. Cell Biol. 126:77-86.
34. Liu, Y., D. Peter, A. Roghani, S. Schuldiner, G.G. Prive, D. Eisenberg, N. Brecha, and R.H. Edwards. 1992. A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell. 70:539-551.
35. Liu, Y., A. Roghani, and R.H. Edwards. 1992. Gene transfer of a reserpine-sensitive mechanism of resistance to MPP+. Proc. Natl. Acad. Sci. USA. 89:9074-9078.
36. Liu, Y., E.S. Schweitzer, M.J. Nirenberg, V.M. Pickel, C.J. Evans, and R.H. Edwards. 1994. Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC12 cells. J. Cell Biol. 127:1419-1433.
37. Martin, T.F.J. 1994. The molecular machinery for fast and slow neurosecretion. Curr. Opin. Neurobiol. 4:626-632.
38. Maycox, P.R., T. Deckwerth, J.W. Hell, and R. Jahn. 1988. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J. Biol. Chem. 263:15423-15428.
39. Melega, W.P., and B.D. Howard. 1981. Choline and acetylcholine metabolism in PC12 secretory cells. Biochemistry. 20:4477-4483.
40. Melega, W.P., and B.D. Howard. 1984. Biochemical evidence that vesicles are the source of the acetylcholine released from stimulated PC12 cells. Proc. Natl. Acad. Sci. USA. 81:6535-6538.
41. Nirenberg, M.J., Y. Liu, D. Peter, R.H. Edwards, and V.M. Pickel. 1995. The vesicular monoamine transporter-2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei. Proc. Natl. Acad. Sci. USA. 92:8773-8777.
42. Nirenberg, M.J., J. Chan, Y. Liu, R.H. Edwards, and V.M. Pickel. 1996. Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine. J. Neurosci. 16:4135-4145.
43. Ohno, H., J. Stewart, M.C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J.S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 269:1872-1875.
44. Orci, L., M. Ravazzola, M. Amherdt, D. Louvard, and A. Perrelet. 1985. Clathrin-immunoreactive sites in the Golgi apparatus are concentrated at the trans pole in polypeptide hormone-secreting cells. Proc. Natl. Acad. Sci. USA. 82:5385-5389.
45. Parsons, S.M., C. Prior, and I.G. Marshall. 1993. Acetylcholine transport, storage and release. Int. Rev. Neurobiol. 35:279-390.
46. Peter, D., Y. Liu, C. Sternini, R. de Giorgio, N. Brecha, and R.H. Edwards. 1995. Differential expression of two vesicular monoamine transporters. J. Neurosci. 15:6179-6188.
47. Regnier-Vigouroux, A., S.A. Tooze, and W.B. Huttner. 1991. Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO (Eur. Mol. Biol. Organ.) J. 10:3589-3601.
48. Roghani, A., J. Feldman, S.A. Kohan, A. Shirzadi, C.B. Gundersen, N. Brecha, and R.H. Edwards. 1994. Molecular cloning of a putative vesicular transporter for acetylcholine. Proc. Natl. Acad. Sci. USA. 91:10620-10624.
49. Schubert, D., and F.G. Klier. 1977. Storage and release of acetylcholine by a clonal cell line. Proc. Natl. Acad. Sci. USA. 74:5184-5188.
50. Schuldiner, S., A. Shirvan, and M. Linial. 1995. Vesicular neurotransmitter transporters: from bacteria to humans. Physiol. Rev. 75:369-392.
51. Sollner, T., and J.E. Rothman. 1994. Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci. 17:344-348.
52. Stinchombe, J.C., and W.B. Huttner. 1994. Purification of secretory granules from PC12 cells. In Cell Biology: A Laboratory Handbook. Vol. 1. J.E. Celis, editor. Academic Press, San Diego. 557-566.
53. Südhof, T.C., P. De Camilli, H. Niemann, and R. Jahn. 1993. Membrane fusion machinery: insights from synaptic proteins. Cell. 75:1-4.
54. Takei, K., O. Mundigl, L. Daniell, and P. De Camilli. 1996. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133:1237-1250.
55. Thureson-Klein, A. 1983. Exocytosis from large and small dense cored vesicles in noradrenergic nerve terminals. Neuroscience. 10:245-259.
56. Tooze, J., and S.A. Tooze. 1986. Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J. Cell Biol. 103:839-850.
57. Tooze, S.A., E. Chanat, J. Tooze, and W.B. Huttner. 1993. Secretory granule formation. In Mechanisms of Intracellular Trafficking and Processing of Proproteins. CRC Press, Boca Raton, FL. 157-177.
58. Varoqui, H., and J.D. Erickson. 1996. Active transport of acetylcholine by the human vesicular acetylcholine transporter. J. Biol. Chem. 271:27229-27232.
59. Walter, P., and A.E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119.
60. Weihe, E., M.K. Schafer, J.D. Erickson, and L.E. Eiden. 1994. Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. J. Mol. Neurosci. 5:149-164.
61. Weihe, E., J.-H. Tao-Cheng, M.K.-H. Schafer, J.D. Erickson, and L.E. Eiden. 1996. Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc. Natl. Acad. Sci. USA. 93:3547-3552.