Kinesin- and myosin-driven steps of vesicle recruitment for Ca2+- regulated exocytosis

Journal of Cell Biology

Volumn 138, Issue 5, 1997, Pages 999-1008

  Bi, Guo Qiang ^a,c   Morris, Robert L ^b   Liao, Guochun ^a   Alderton, Janet M ^a   Scholey, Jonathan M ^b   Steinhardt, Richard A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; ENZYME INHIBITOR; KINESIN; MICROTUBULE PROTEIN; MYOSIN; PROTEIN KINASE (CALCIUM,CALMODULIN);

ARTICLE; CELL MEMBRANE TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PURIFICATION; ESCHERICHIA COLI; EXOCYTOSIS; GENE EXPRESSION; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; ANTIBODIES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELL MEMBRANE; CLONING, MOLECULAR; COATED VESICLES; DIACETYL; ENZYME INHIBITORS; EXOCYTOSIS; FEMALE; KINESIN; KINETICS; MALE; MYOSINS; OVUM; RECOMBINANT PROTEINS; SEA URCHINS; SPERMATOZOA; TIME FACTORS;

ESCHERICHIA COLI;

EID: 0030984076     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.138.5.999     Document Type: Article

References (68)

1. Adams, R.J., and T.D. Pollard. 1986. Propulsion of organelles isolated from Acanthamoeba along actin filaments by myosin-I. Nature (Lond.). 322:754-756.
2. Allan, V. 1995. Membrane traffic motors. FEBS Lett. 369:101-106.
3. 2+/calmodulin-dependent protein kinase is necessary for nuclear envelope breakdown. J. Cell Biol. 111:1763-1773.
4. Bearer, E.L., J.A. DeGiorgis, N.A. Medeiros, and T.S. Reese. 1996. Actin-based motility of isolated axoplasmic organelles. Cell Motil Cytoskel. 33:106-114.
5. Bennett, M.K., and R.H. Scheller. 1994. Molecular correlates of synaptic vesicle docking and fusion. Curr. Opin. Neurobiol. 4:324-329.
6. Betz, W.J., and G.S. Bewick. 1992. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science (Wash. DC). 255:200-203.
7. Betz, W.J., and L.G. Wu. 1995. Synaptic transmission. Kinetics of synaptic-vesicle recycling. Curr. Biol. 5:1098-1101.
8. Bi, G.Q., J.M. Alderton, and R.A. Steinhardt. 1995. Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131:1747-1758.
9. Bloom, G.S., and S.A. Endow. 1995. Motor proteins 1: kinesins. Protein Profile. 2:1105-1171.
10. Borges, S., E. Gleason, M. Turelli, and M. Wilson. 1995. The kinetics of quantal transmitter release from retinal amacrine cells. Proc. Natl. Acad. Sci. USA. 92:6896-6900.
11. Brady, S.T., K.K. Pfister, and G.S. Bloom. 1990. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc. Natl. Acad. Sci. USA. 87:1061-1065.
12. Ceccaldi, P.E., F. Grohovaz, F. Benfenati, E. Chieregatti, P. Greengard, and F. Valtorta. 1995. Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. J. Cell Biol. 128:905-912.
13. 2+ triggers massive exocytosis in Chinese hamster ovary cells. EMBO (Eur. Mol. Biol. Organ.) J. 15: 3787-3791.
14. Cramer, L.P., and T.J. Mitchison. 1995. Myosin is involved in postmitotic cell spreading. J. Cell Biol. 131:179-189.
15. Dan, Y., and M.M. Poo. 1992. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature (Lond.). 359:733-736.
16. De Camilli, P. 1995. The eighth Datta Lecture. Molecular mechanisms in synaptic vesicle recycling. FEBS Lett. 369:3-12.
17. Drubin, D.G., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
18. Path, K.R., and D.R. Burgess. 1994. Membrane motility mediated by unconventional myosin. Curr. Opin. Cell Biol. 6:131-135.
19. Fath, K.R., G.M. Trimbur, and D.R. Burgess. 1994. Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126:661-675.
20. 2+/calmodulin-and cAMP-dependent protein kinases in vitro. J. Neurosci. 15:2385-2395.
21. Gho, M., K. McDonald, B. Ganetzky, and W.M. Saxton. 1992. Effects of kinesin mutations on neuronal functions. Science (Wash. DC). 258:313-316.
22. Girod, R., S. Popov, J. Alder, J.Q. Zheng, A. Lohof, and M.M. Poo. 1995. Spontaneous quantal transmitter secretion from myocytes and fibroblasts: comparison with neuronal secretion. J. Neurosci. 15:2826-2838.
23. Goldstein, L.S. 1993. With apologies to Scheherazade: tails of 1001 kinesin motors. Annu. Rev. Genet. 27:319-351.
24. 2+-sensitive streaming in the alga Chara: detection of two polypeptides reacting with a monoclonal anti-myosin and their localization in the streaming endoplasm. Eur. J. Cell Biol. 47:22-31.
25. Hasson, T., and M.S. Mooseker. 1995. Molecular motors, membrane movements and physiology: emerging roles for myosins. Curr. Opin. Cell Biol. 7:587-594.
26. Hirling, H., and R.H. Scheller. 1996. Phosphorylation of synaptic vesicle proteins: modulation of the alpha SNAP interaction with the core complex. Proc. Natl. Acad. Sci. USA. 93:11945-11949.
27. Hirokawa, N., K.K. Pfister, H. Yorifuji, M.C. Wagner, S.T. Brady, and G.S. Bloom. 1989. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell. 56:867-878.
28. Hollenbeck, P.J., and W.Z. Cande. 1985. Microtubule distribution and reorganization in the first cell cycle of fertilized eggs of Lytechinus pictus. Eur. J. Cell Biol. 37:140-148.
29. Hollenbeck, P.J., and J.A. Swanson. 1990. Radial extension of macrophage tubular lysosomes supported by kinesin. Nature (Lond.). 346:864-866.
30. Ingold, A.L., S.A. Cohn, and J.M. Scholey. 1988. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J. Cell Biol. 107:2657-2667.
31. Johnston, G.C., J.A. Prendergast, and R.A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539-551.
32. Kumar, J., H. Yu, and M.P. Sheetz. 1995. Kinectin, an essential anchor for kinesin-driven vesicle motility. Science (Wash. DC). 267:1834-1837.
33. Kuznetsov, S.A., G.M. Langford, and D.O. Weiss. 1992. Actin-dependent organelle movement in squid axoplasm. Nature (Lond.). 356:722-725.
34. Langford, G.M. 1995. Actin-and microtubule-dependent organelle motors: interrelationships between the two motility systems. Curr. Opin. Cell Biol. 7:82-88.
35. Langford, G.M., S.A. Kuznetsov, D. Johnson, D.L. Cohen, and D.G. Weiss. 1994. Movement of axoplasmic organelles on actin filaments assembled on acrosomal processes: evidence for a barbed-end-directed organelle motor. J. Cell Sci. 107:2291-2298.
36. Lin, C.H., E.M. Espreafico, M.S. Mooseker, and P. Forscher. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron. 16:769-782.
37. Llinas, R., J.A. Gruner, M. Sugimori, T.L. McGuinness, and P. Greengard. 1991. Regulation by synapsin I and Ca(2+)-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. J. Physiol. 436:257-282.
38. Miller, M., E. Bower, P. Levitt, D. Li, and P.D. Chantier. 1992. Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization. Neuron. 8:25-44.
39. Miyake, K., and P.L. McNeil. 1995. Vesicle accumulation and exocytosis at sites of plasma membrane disruption. J. Cell Biol. 131:1737-1745.
40. Mochida, S., H. Kobayashi, Y. Matsuda, Y. Yuda, K. Muramoto, and Y. Nonomura. 1994. Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron. 13:1131-1142.
41. Morris, R.L., and P.J. Hollenbeck. 1995. Axonal transport of mitochondria along microlubules and F-actin in living vertebrate neurons. J. Cell Biol. 131: 1315-1326.
42. Neher, E., and R.S. Zucker. 1993. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron. 10:21-30.
43. Nielander, H.B., F. Onofri, F. Valtorta, G. Schiavo, C. Montecucco, P. Greengard, and F. Benfenati. 1995. Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J. Neurochem. 65:1712-1720.
44. Pieribone, V.A., O. Shupliakov, L. Brodin, S. Hilfiker-Rothenfluh, A.J. Czernik, and P. Greengard. 1995. Distinct pools of synaptic vesicles in neurotransmitter release [see comments]. Nature (Lond.). 375:493-497.
45. 2+/calmodulin protein kinase II in synaptic vesicles. FEBS Lett. 317:85-88.
46. Popoli, M., A. Venegoni, C. Vocaturo, L. Buffa, J. Perez, E. Smeraldi, and G. Racagni. 1997. Long-term blockade of serotonin reuptake affects synaptotagmin phosphorylation in the hippocampus. Mol. Pharm. 51:19-26.
47. Porter, M.E., J.M. Scholey, D.L. Stemple, G.P. Vigers, R.D. Vale, M.P. Sheetz, and J.R. McIntosh. 1987. Characterization of the microtubule movement produced by sea urchin egg kinesin. J. Biol. Chem. 262:2794-2802.
48. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137:93-104.
49. Rodionov, V.I., F.K. Gyoeva, and V.I. Gelfand. 1991. Kinesin is responsible for centrifugal movement of pigment granules in melanophores. Proc. Natl. Acad. Sci. USA. 88:4956-4960.
50. Rosahl, T.W., D. Spillane, M. Missler, J. Herz, D.K. Selig, J.R. Wolff, R.E. Hammer, R.C. Malenka, and T.C. Sudhof. 1995. Essential functions of synapsins I and II in synaptic vesicle regulation [see comments]. Nature (Lond). 375:488-493.
51. Rosenmund, C., and C.F. Stevens. 1996. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron. 16:1197-1207.
52. Ryan, T.A., H. Reuter, B. Wendland, F.E. Schweizer, R.W. Tsien, and S.J. Smith. 1993. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron. 11:713-724.
53. Saxton, W.M., J. Hicks, L.S. Goldstein, and E.C. Raff. 1991. Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell. 64:1093-1102.
54. Scholey, J.M. 1996. Kinesin-II, a membrane traffic motor in axons, axonemes, and spindles. J. Cell Biol. 133:1-4.
55. Scholey, J.M., M.E. Porter, P.M. Grissom, and J.R. McIntosh. 1985. Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature (Lond.). 318:483-486.
56. Skoufias, D.A., D.G. Cole, K.P. Wedaman, and J.M. Scholey. 1994. The carboxyl-terminal domain of kinesin heavy chain is important for membrane binding. J. Biol. Chem. 269:1477-1485.
57. Steinhardt, R. A., G. Bi, and J.M. Alderton. 1994. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science (Wash. DC). 263:390-393.
58. Stevens, C.F., and T. Tsujimoto. 1995. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc. Natl. Acad. Sci. USA. 92:846-849.
59. Sudhof, T.C., P. De Camilli, H. Niemann, and R. Jahn. 1993. Membrane fusion machinery: insights from synaptic proteins. Cell. 75:1-4.
60. Terasaki, M. 1995. Visualization of exocytosis during sea urchin egg fertilization using confocal microscopy. J. Cell Sci. 108:2293-2300.
61. Vale, R.D., T.S. Reese, and M.P. Sheetz. 1985a. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 42: 39-50.
62. Vale, R.D., B.J. Schnapp, T. Mitchison, E. Steuer, T.S. Reese, and M.P. Sheetz. 1985b. Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell. 43:623-632.
63. Vallee, R.B., and M.P. Sheetz. 1996. Targeting of motor proteins. Science (Wash. DC). 271:1539-1544.
64. Waxham, M.N., R.C. Malenka, P.T. Kelly, and M.D. Mauk. 1993. Calcium/ calmodulin-dependent protein kinase II regulates hippocampal synaptic transmission. Brain Res. 609:1-8.
65. Wright, B.D., J.H. Henson, K.P. Wedaman, P.J. Willy, J.N. Morand, and J.M. Scholey. 1991. Subcellular localization and sequence of sea urchin kinesin heavy chain: evidence for its association with membranes in the mitotic apparatus and interphase cytoplasm [published erratum appears 114:following 863]. J. Cell Biol. 113:817-833.
66. Wright, B.D., M. Terasaki, and J.M. Scholey. 1993. Roles of kinesin and kinesin-like proteins in sea urchin embryonic cell division: evaluation using antibody microinjection. J. Cell Biol. 123:681-689.
67. Yang, J.T., R.A. Laymon, and L.S. Goldstein. 1989. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses. Cell. 56:879-889.
68. Yang, J.T., W.M. Saxton, R.J. Stewart, E.C. Raff, and L.S. Goldstein. 1990. Evidence that the head of kinesin is sufficient for force generation and motility in vitro. Science (Wash. DC). 249:42-47.