Calcium binds dynamin I and inhibits its GTPase activity

Journal of Neurochemistry

Volumn 66, Issue 5, 1996, Pages 2074-2081

  Liu, Jun Ping ^a,d   Zhang, Qun Xing ^b   Baldwin, Graham ^c   Robinson, Phillip J ^a  

^a JOHN HUNTER HOSPITAL   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

^c AUSTIN HOSPITAL   (Australia)

^d BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Calcium; Dynamin; Neurotransmission; Phosphorylation; Protein kinase C; Synaptic vesicle recycling

Indexed keywords

CALCIUM; DYNAMIN; GUANOSINE TRIPHOSPHATASE;

ANIMAL TISSUE; ARTICLE; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME INHIBITION; MEMBRANE DEPOLARIZATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

EID: 0029888020     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.66052074.x     Document Type: Article

References (44)

1. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
2. Chen M. S., Obar R. A., Schroeder C. C., Austin T. W., Poodry C. A., Wadsworth S. C., and Vallee R. B. (1991) Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
3. Cook T. A., Urrutia R., and McNiven M. A. (1994) Identification of dynamin 2, an isoform ubiquitously expressed in rat tissues. Proc. Natl. Acad. Sci. USA 91, 644-648.
4. 2+ overlay of protein blots. Anal. Biochem. 194, 82-88.
5. Gout I., Dhand R., Hiles I. D., Fry M. J., Panayotou G., Das P., Truong O., Totty N. F., Hsuan J., Booker G. W., Campbell I. D., and Waterfield M. D. (1993) The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25-36.
6. Haslam R. J., Koide H. B., and Hemmings B. A. (1993) Pleckstrin domain homology. Nature 363, 309-310.
7. Herskovits J. S., Burgess C. C., Obar R. A., and Vallee R. B. (1993a) Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578.
8. Herskovits J. S., Shpetner H. S., Burgess C. C , and Vallee R. B. (1993b) Microtubles and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain. Proc. Natl. Acad. Sci. USA 90, 11468-11472.
9. Hess S. D., Doroshenko P. A., and Augustine G. J. (1993) A functional role for GTP-binding proteins in synaptic vesicle cycling. Science 259, 1169-1172.
10. Hinshaw J. E. and Schmid S. L. (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding [see comments]. Nature 374, 190-192.
11. Knoll G., Plattner H., and Nordmann J. J. (1992) Exo-endocytosis in isolated peptidergic nerve terminals occurs in the subsecond range. Biosci. Rep. 12, 495-501.
12. Kosaka T. and Ikeda K. (1983) Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14, 207-225.
13. Krueger B. K., Forn J., and Greengard P. (1977) Depolarization-induced phosphorylation of specific proteins, mediated by calcium ion influx, in rat brain synaptosomes. J. Biol. Chem. 252, 2764-2773.
14. Liu J.-P. (1996) Protein kinase C and its substrates. Mol. Cell. Endocrinol. 116, 1-29.
15. Liu J.-P. and Robinson P. J. (1995) Dynamin and endocytosis. Endocr. Rev. 16, 590-607.
16. Liu J.-P., Powell K. A., Südhof T. C., and Robinson P. J. (1994a) Dynamin is a calcium-sensitive phospholipid-binding protein with very high affinity for protein kinase C. J. Biol. Chem. 269, 21043-21050.
17. Liu J.-P., Sim A. T. R., and Robinson P. J. (1994b) Calcineurin inhibition of dynamin I GTPase activity is coupled to nerve terminal depolarization. Science 265, 970-973.
18. Maeda K., Nakata T., Noda Y., Sato-Yoshitake R., and Hirokawa N. (1992) Interaction of dynamin with microtubules: its structure and GTPase activity investigated by using highly purified dynamin. Mol. Biol. Cell 3, 1181-1194.
19. McPherson P. S., Takei K., Schmid S. L., and De Camilli P. (1994) p145, a major grb2-binding protein in brain, is co-localized with dynamin in nerve terminals where it undergoes activity-dependent dephosphorylation. J. Biol. Chem. 269, 30132-30139.
20. h: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264, 1593-1596.
21. Nakata T., Takemura R., and Hirokawa N. (1993) A novel member of the dynamin family of GTP-binding proteins is expressed specifically in the testis. J. Cell Sci. 105, 1-5.
22. 2+-dependent steps in chromaffin cell secretion. Neuron 10, 21-30.
23. Noda Y., Nakata T., and Hirokawa N. (1993) Localization of dynamin: widespread distribution in mature neurons and association with membranous organelles. Neuroscience 55, 113-127.
24. Obar R. A., Collins C. A., Hammarback J. A., Shpetner H. S., and Vallee R. B. (1990) Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347, 256-261.
25. Otsu M., Hiles I., Gout I., Fry M. J., Ruiz-Larrea F., Panayotou G., Thompson A., Dhand R., Hsuan J., Totty N., et al. (1991) Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes, and PI3-kinase. Cell 65, 91-104.
26. Powell K. A. and Robinson P. J. (1995) Dephosphin/dynamin is a neuronal phosphoprotein concentrated in nerve terminals: evidence from rat cerebellum. Neuroscience 64, 821-833.
27. Ramaswami M., Krishnan K. S., and Kelly R. B. (1994) Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13, 363-375.
28. Robinson P. J. (1992) Differential stimulation of protein kinase C activity by phorbol ester or calcium/phosphatidylserine in vitro and in intact synaptosomes. J. Biol. Chem. 267, 21637-21644.
29. Robinson P. J. and Dunkley P. R. (1983) Depolarisation-dependent protein phosphorylation in rat cortical synaptosomes: factors determining the magnitude of the response. J. Neurochem. 41, 909-918.
30. Robinson P. J., Sontag J.-M., Liu J.-P., Fykse E M., Slaughter C., McMahon H., and Südhof T. C. (1993) Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 163-166.
31. Robinson P. J., Liu J.-P., Powell K. A., Fykse E. M., and Südhof T. C. (1994) Phosphorylation of dynamin I and synaptic vesicle recycling. Trends Neurosci. 17, 348-353.
32. Ryan T. A., Reuter H., Wendland B., Schweizer F. E., Tsien R. W., and Smith S. J. (1993) The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
33. Shpetner H. S. and Vallee R. B. (1989) Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59, 421-432.
34. Shpetner H. S. and Vallee R. B. (1992) Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature 355, 733-735.
35. Sontag J.-M., Fykse E. M., Ushkaryov Y., Liu J.-P., Robinson P. J., and Südhof T. C. (1994) Differential expression and regulation of multiple dynamins. J. Biol. Chem. 269, 4547-4554.
36. Takel K., McPherson P. S., Schmid S. L., and De Camilli P. (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals [see comments]. Nature 374, 186-190.
37. Thomas P., Lee A. K., Wong J. G., and Almers W. (1994) A triggered mechanism retrieves membrane in seconds after Ca(2+)-stimulated exocytosis in single pituitary cells. J. Cell Biol. 124, 667-675.
38. Tse A., Tse F. W., Almers W., and Hille B. (1993) Rhythmic exocytosis stimulated by GnRH-induced calcium oscillations in rat gonadotropes. Science 260, 82-84.
39. Tuma P. L. and Collins C. A. (1994) Activation of dynamin GTPase is a result of positive cooperativity. J. Biol. Chem. 269, 30842-30847.
40. Tuma P. L., Stachniak M. C., and Collins C. A. (1993) Activation of dynamin GTPase by acidic phospholipids and endogenous rat brain vesicles. J. Biol. Chem. 268, 17240-17246.
41. Vallee R. B. and Shpetner H. S. (1990) Motor proteins of cytoplasmic microtubules. Annu. Rev. Biochem. 59, 909-932.
42. Van der Bliek A M. and Meyerowitz E. M. (1991) Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
43. Van der Bliek A. M., Redelmeier T. E., Damke H., Tisdale E. J., Meyerowitz E. M., and Schmid S. L. (1993) Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553-563.
44. von Gersdorff H. and Matthews G. (1994) Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652-655.