EGFP-tagged vasopressin precursor protein sorting into large dense core vesicles and secretion from PC12 cells

Cellular and Molecular Neurobiology

Volumn 25, Issue 3-4, 2005, Pages 581-605

  Zhang, Bing Jun ^a,b   Yamashita, Mitsuo ^a,c   Fields, Ray ^a   Kusano, Kiyoshi ^a   Gainer, Harold ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b MCMASTER UNIVERSITY   (Canada)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Exocytosis; Green fluorescent protein; Neurophysin; Regulated secretory pathway; Vasopressin

Indexed keywords

AMINO ACID; CHAPERONE; DNA; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NEUROPHYSIN; PROTEIN PRECURSOR; UNCLASSIFIED DRUG; VASOPRESSIN; VASOPRESSIN PRECURSOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL SECRETION; CELL STRAIN; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE; FLUORESCENCE MICROSCOPY; GENE CONSTRUCT; GENE DELETION; GENETIC TRANSFECTION; HORMONE RELEASE; IMAGING; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN TARGETING; RAT; REPORTER GENE; SECRETORY VESICLE;

ANIMALS; CYTOPLASM; EXOCYTOSIS; EXONS; GREEN FLUORESCENT PROTEINS; MICROSCOPY, IMMUNOELECTRON; MOLECULAR CHAPERONES; NEURONS; NEUROPHYSINS; PC12 CELLS; PROTEIN PRECURSORS; RATS; SECRETORY VESICLES; TRANSFECTION; VASOPRESSINS;

EID: 23944520877     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-005-3970-x     Document Type: Article

References (66)

1. Acher, R., Light, A., and DuVigneaud, V. (1958). Purification of oxytocin and vasopressin by way of a protein complex. J. Biol. Chem. 233:116-120.
2. Angleson, J. K., Cochilla, A. J., Kilie, G., Nussinovitch, I., and Betz, W. T. (1999). Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytotic events. Nat. Neurosci. 2:440-444.
3. Arvan, P., and Castle, D. (1998). Sorting and storage during secretory granule biogenesis: Looking backward and looking forward. Biochem. J. 332:592-610.
4. Belenky, M., Castel, M., Young, W. S., Gainer, H., and Cohen, S. (1992). Ultrastructural immunolocalization of rat oxytocin-neurophysin in transgenic mice expressing the rat oxytocin gene. Brain Res. 583:279-286.
5. Ben-Barak, Y., Russell, J. T., Whitnall, M. H., Ozato, K., and Gainer, H. (1985). Neurophysin in the hypothalamoneurohypophysial system. I. Production and characterization of monoclonal antibodies. J. Neurosci. 5:81-97.
6. Breslow, E., and Burman, S. (1990). Molecular, thermodynamic, and biological aspects of recognition and function in neurophysin-hormone systems. A model system for the analysis of protein-peptide interactions. Adv. Enzymol. 63:1-67.
7. Brownstein, M. J., Russell, J. T., and Gainer, H. (1980). Synthesis, transport, and release of posterior pituitary hormones. Science 207:373-378.
8. Buma, P., and Nieuwenhuys, R. (1987). Ultrastructural demonstration of ocytocin and vasopressin release sites in the neural lobe and median eminence of the rat by tannic acid and immunogold methods. Neurosci. Lett. 74:151-157.
9. Buma, P., and Roubos, E. E. (1983). Calcium dynamics, exocytosis, and membrane turnover in the ovulation hormone-releasing Caudo-Dorsal-Cells of Lymnaea stagnalis. Cell Tissue Res. 233:143-159.
10. Buma, P., Roubos, E. W., and Buijs, R. M. (1984). Ultrastructural demonstration of exocytosis of neural, neuroendocrine and endocrine secretions with an in vitro tannic acid (TARI-) method. Histochemistry 80:247-256.
11. Burbach, J. P. H., Luckman, S. M., Murphy, D., and Gainer, H. (2001). Gene regulation in the magnocellular hypothalamo-neurohypophysial system. Physiol. Rev. 81:1197-1267.
12. Burgess, T. L., and Kelly, R. B. (1987). Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:243-293.
13. Burke, N. V., Han, W., Li, D., Takimoto, K., Watkins, S. C., and Levitan, E. S. (1997). Neuronal peptide release is limited by secretory granule mobility. Neuron 19:1095-1102.
14. Castel, M., Morris, J., and Belenky, M. (1996). Non-synaptic and dendritic exocytosis from dense-coredvesicles in the suprachiasmatic nucleus. NeuroReport 7:543-547.
15. Castel, M., Morris, J., Ben-Barak, Y., Timberg, R., Sivan, N., and Gainer, H. (1985). Ultrastructural localization of immunoreactive neurophysins using monoclonal antibodies and protein A-gold. J. Histochem. Cytochem. 33:1015-1025.
16. Chaiken, I. M., Tamaoki, H., Brownstein, M. J., and Gainer, H. (1983). Onset of neurophysin self-association upon neurophysin/neuropeptide hormone precursor biosynthesis. FEBS Lett. 164:361-365.
17. Chen, L. Q., Rose, J. P., Breslow, E., Yang, D., Chang, W. R., Furey, W. F., Jr., Sax, M., and Wang, B. C. (1991). Crystal structure of a bovine neurophysin II dipeptide complex at 2.8 A determined from the single-wavelength anomalous scattering signal of an incorporated iodine atom. Proc. Natl. Acad. Sci. USA 88:4240-4244.
18. Dannies, P. S. (1999). Protein hormone storage in secretory granules: Mechanisms for concentration and sorting. Endocrinol. Rev. 20:3-21.
19. de Bree, F. M. (2000). Trafficking of the vasopressin and oxytocin prohormone through the regulated secretory pathway. J. Neuroendocrinol. 12:589-594.
20. de Bree, F. M., and Burbach, J. P. H. (1994). Heterologous biosynthesis and processing of prepro vasopressin Neuro 2A neuroblastoma cells. Biochimie 76:265-270.
21. de Bree, F. M., and Burbach, J. P. H. (1998). Structure-function relationship of the vasopressin prohormone domains. Cell. Mol. Neurobiol. 18:173-191.
22. de Bree, F. M., Knight, D., Howell, L., and Murphy, D. (2000). Sorting of the vasopressin prohormone into the regulated secretory pathway. FEBS Lett. 475:175-180.
23. Fricker, L. D. (1988). Carboxypeptidase E. Annu. Rev. Physiol. 50:309-321.
24. Futaesaku, Y., Mizuhira, V., and Nakamura, H. (1972). The new fixation method using tannic acid for electron microscopy and some observations of biological specimens. Proc. Int. Congr. Histochem. Cytochem. 4:155-158.
25. Gainer, H., and Wray, S. (1994). Cellular and molecular biology of oxytocin and vasopressin. In Knobil, E., and Neill, J. D. (ed.). The Physiology of Reproduction. Raven Press, New York, pp. 1099-1129.
26. Greene, L. A., and Rein, G. (1977a). Release, storage and uptake of catecholamines by a clonal cell line of nerve growth factor (NGF) responsive pheochromocytoma cells. Brain Res. 129:247-263.
27. Greene, L. A., and Rein, G. (1977b). Release of [3H] norepinephrine from a clonal line of pheochromocytoma cells (PC12) by nicotinic cholinergic stimulation. Brain Res. 138:521-528.
28. Greene, L. A., and Tischer, A. S. (1976). Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Nat'l. Acad. Sci. USA 73:2424-2428.
29. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3350.
30. 2+-induced deprotonation of peptide hormones inside secretory vesicles in preparation for release. J. Neurosci. 19:900-905.
31. Han, W., Ng, Y-K., Axelrod, D., and Levitan, E. S. (1999b). Neuropeptide release by efficient recruitment of diffusing cytoplasmic secretory vesicles. Proc. Natl. Acad. Sci. U.S.A. 96:14577-14582.
32. Hara, Y., Battey, J., and Gainer, H. (1990). Structure of mouse vasopressin and oxytocin genes. Mol. Brain Res. 8:319-324.
33. House, S. B., Thomas, A., Kusano, K., and Gainer, H. (1998). Stationary organotypic ultures of oxytocin and vasopressin magnocellular neurons from rat and mouse hypothalamus. J. Neuroendocrinol. 10:849-861.
34. Kaether, C., Salm, T., Glombik, M., Almers, W., and Gerdes, H-H. (1997). Targeting of green fluorescent protein to neuroendocrine secretory granules: A new tool for real time studies of regulated protein secretion. Eur. J. Cell Biol. 74:133-142.
35. 2+ compounds. J. Physiol. (Lond.) 494:53-65.
36. Kasai, H., Kishimoto, T., Lui, T. T., Miyashita, Y., Podini, P., Grohovax, F., and Meldolesi, J. (1999). Multiple and diverse forms of regulated exocytosis in wild-type and defective PC12 cells. Proc. Natl. Acad. Sci. U.S.A. 96:945-949.
37. Kanmera, T., and Chaiken, I. M. (1985). Molecular properties of the oxytocin/bovine neurophysin biosynthetic precursor. J. Biol. Chem. 260:8474-8482.
38. Kelly, R. B. (1993). Storage and release of neurotransmitters. Cell 72:45-53.
39. 2+-triggered peptide secretion in single cells image with green fluorescent protein and evanescent-wave microscopy. Neuron 18:857-863.
40. Loh, Y. P., Snell, C. R., and Cool, D. R. (1997). Receptor-mediated targeting of hormones to secretory granules: Role of carboxypeptidase E. Trends Endocrinol. Metab. 8:130-137.
41. 2+ and neurotransmitter release: Studies on PC12 cells and synaptosomes exposed to a-latrotoxin. Proc. Natl. Acad. Sci. U.S.A. 81:620-624.
42. Morris, J. F., and Pow, D. V. (1988) Capturing and quantifying the exocytotic event. J. Exp. Biol. 139:81-103.
43. Nakamura, N., Lowe, M., Levine, T. P., Rabouille, C., and Warren, G. (1997). The vesicle docking protein P115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell 89:445-455.
44. Neumann, I., Russell, J. A., and Landgraf, R. (1993). Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: A microdialysis study. Neuroscience 53:65-75.
45. Noteborn, H. P. J. M., Roubos, E. W., Ebels, I., Ven, van de A. M. H., and Buma, P. (1986). Ultrastructural demonstration by exocytosis in rat pinealocytes with the use of the tannic acid method. Cell Tissue Res. 245:223-225.
46. O'Lague, P. H., Huttner, S. L., Vandenberg, C. A., Morrison-Graham, K., and Horn, R. (1985). Morphological properties and membrane channels of the growth cones induced in PC12 cells by nerve growth factor. J. Neurosi. Res. 13:301-321.
47. Patterson, G. H., Magnuson, M. A., and Piston, D. W. (1996). Confocal microscopy studies of secretion using insulin-green fluorescent protein. Biophys. J. 70:A426.
48. Pickering, B. T., and Jones, C. W. (1978). The neurophysins. Hormon. Proteins Pept. 5:103-158.
49. 2+-dependent and-independent release of neurotransmitters from PC12 cells: A role for protein kinase C activation? J. Cell Biol. 99:628-638.
50. Rose, J. P., Wu, C. K., Hsiao, C. D., Breslow, E., and Wang, B. C. (1996). Crystal structure of the neurophysin-oxytocin complex. Nat. Struct. Biol. 3(2):163-169.
51. Roubos, E. W., and Van der Wal-Divendal, R. M. (1980). Ultrastructural Analysis of peptide-hormone release by exocytosis. Cell Tissue Res. 207:267-275
52. 2+ influx in magnocellular vasopressin neurones isolated from rat supraoptic nucleus. J. Physiol. 503:253-268.
53. Shafer, T. J., Atchison, W. D. (1991). Transmitter, ion channel and receptor properties of pheochromocytoma (PC12) cells: A model for neurotoxicological studies. NeuroToxicology 12:473-492.
54. Sladek, C. D. (1999). Antidiuretic hormone: Synthesis and release. In Fray, J. C.S. (ed.). Handbook of Physiology, Section 7, The Endocrine System, Vol. III: Endocrine Regulation of Water and Electrolyte Balance, Oxford University Press, Oxford, UK. pp. 436-495.
55. Tanner, V., Ploug, T., and Tao-Cheng, J.-H. (1996). Subcellular localization of SV2 and other secretory vesicle components in PC12 cells by an efficient method of pre-embedding EM immunocytochemistry for cell cultures. J. Histochem. Cytochem. 144:1481-1488.
56. Tooze, S. A. (1998). Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Bioch. Biophys. Acta. 1401:231-244.
57. Young, W. S. III (1992). Expression of the oxytocin and vasopressin genes. J. Neuroendocrinol. 4:529-540.
58. Young, W. S. III, Iacangelo, A., Luo, X-Z. J., King Duncan, K., Ginns, E. I. (1999). Transgenic expression of green fluorescent protein in mouse oxytocin neurons. J. Neuroendocrinol. 11:935-939.
59. Waller, S., Fairhall, K. M., Xu, J., Robinson, I. C. A. F., and Murphy, D. (1996). Neurohypophysial and fluid homeostasis in transgenic rats expressing a tagged vasopressin prepropeptide in hypothalamic neurons. Endocrinology 137:5068-5077.
60. Wagner, J. A. (1985). Structure of catecholamine secretory vesicles from PC12 cells. J. Neurochem. 45:1244-1253.
61. 2+ channels in vasopressin secretion from neurohypophysial terminals of the rat. J. Physiol. 502:351-363.
62. Weihe, E., Schäfer, M.K-H., Erickson, J. D., and Eiden, L. E. (1994). Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. J. Mol. Neurosci. 5:149-164.
63. Weihe, E., Tao-Cheng, J.-H., Schäfer, M. K.-H., Erickson, J. D., and Eiden, L. E. (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. U.S.A. 93:3547-3552.
64. Westerink, R. H. S., Groot, de A., and Vijverberg, H. P. M. (2000). Heterogeneity of catecholamine-containing vesicles in PC12 cells. Biochem. Biophys. Res. Commun. 270:625-630.
65. Whitnall, M. H., Key, S., Ben-Barak, Y., Ozato, K., and Gainer, H. (1985). Neurophysin in the hypothalamo neurohypophysial system. II. Immunocytochemical studies of the ontogeny of oxytocinergic and vasopressinergic neurons. J. Neurosci. 5:98-109.
66. Zhang, B-J., Kusano, K., Zerfas, P., Iacangelo, A., Young, W. S. III, and Gainer, H. (2002) Targeting of green fluorescent protein to secretory granules in oxytocin magnocellular neurons and its secretion from neurohypophysial nerve terminals in transgenic mice, Endocrinology 143:1036-1046.