Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling

Neuron

Volumn 30, Issue 1, 2001, Pages 197-210

  Krishnan, K S ^b   Rikhy, Richa ^b   Rao, Sujata ^b   Shivalkar, Madhuri ^b   Mosko, Michael ^a   Narayanan, Radhakrishnan ^a   Etter, Paul ^a   Estes, Patricia S ^a   Ramaswami, Mani ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GUANOSINE TRIPHOSPHATE; NUCLEOSIDE DIPHOSPHATE KINASE; NUCLEOSIDE TRIPHOSPHATE;

ALLELE; ARTICLE; DROSOPHILA; ENDOCYTOSIS; GENE MUTATION; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; INTERNALIZATION; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SYNAPSE VESICLE; TEMPERATURE SENSITIVITY; TUMOR SUPPRESSOR GENE;

EID: 0035036343     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(01)00273-2     Document Type: Article

References (83)

1. Alawi A.A., Pak W.L. On-transient of insect electroretinogram. its cellular origin Science. 172:1971;1055-1057.
2. Baba H., Urano T., Okada K., Furukawa K., Nakayama E., Tanaka H., Iwasaki K., Shiku H. Two isotypes of murine nm23/nucleoside diphosphate kinase, nm23-M1 and nm23-M2, are involved in metastatic suppression of a murine melanoma line. Cancer Res. 55:1995;1977-1981. a.
3. Baba T., Damke H., Hinshaw J.E., Ikeda K., Schmid S.L., Warnock D.E. Role of dynamin in clathrin-coated vesicle formation. Cold Spring Harb. Symp. Quant. Biol. 60:1995;235-242. b.
4. Babst M., Odorizzi G., Estepa E., Emr S. Mammalian TSG101 and the yeast homologue Vps23p, both function in late endosomal trafficking. Traffic. 1:2000;248-258.
5. Betz W.J., Bewick G.S. Optical analysis of synaptic vesicle cycling at the frog neuromuscular junction. Science. 255:1992;200-203.
6. Biggs J., Tripoulas N., Hersperger E., Dearolf C., Shearn A. Analysis of the lethal interaction between the prune and Killer of prune mutations of Drosophila. Genes Dev. 2:1988;1333-1343.
7. Biggs J., Hersperger E., Steeg P.S., Liotta L.A., Shearn A. A Drosophila gene that is homologous to a mammalian gene associated with tumor metastasis codes for a nucleoside diphosphate kinase. Cell. 63:1990;933-940.
8. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily. a conserved switch for diverse cell functions Nature. 348:1990;125-132.
9. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily. conserved structure and molecular mechanism Nature. 349:1991;117-127.
10. Chen Y.S., Obar R.A., Schroeder C.C., Austin T.W., Poodry C.A., Wadsworth S.C., Vallee R.B. Multiple forms of dynamin are encoded by the shibire, a Drosophila gene involved in endocytosis. Nature. 351:1991;583-586.
11. Cremona O., De Camilli P. Synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 7:1997;323-330.
12. Damke H., Baba T., Warnock D.E., Schmid S.L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:1994;915-934.
13. De Camilli P., Takei K. Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron. 16:1996;481-486.
14. Dearolf C.R., Hersperger E., Shearn A. Developmental consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev. Biol. 129:1988;159-168. a.
15. Dearolf C.R., Tripoulas N., Biggs J., Shearn A. Molecular consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev. Biol. 129:1988;169-178. b.
16. Engel M., Veron M., Theisinger B., Lacombe M.L., Seib T., Dooley S., Welter C. A novel serine/threonine-specific protein phosphotransferase activity of Nm23/nucleoside-diphosphate kinase. Eur. J. Biochem. 234:1995;200-207.
17. Engel M., Seifert M., Theisinger B., Seyfert U., Welter C. Glyceraldehyde-3-phosphate dehydrogenase and Nm23-H1/nucleoside diphosphate kinase A. Two old enzymes combine for the novel Nm23 protein phosphotransferase function. J. Biol. Chem. 273:1998;20058-20065.
18. Estes P.S., Roos J., van der Bliek A., Kelly R.B., Krishnan K.S., Ramaswami M. Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J. Neurosci. 16:1996;5443-5456.
19. Fish K.N., Schmid S.L., Damke H. Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell. Biol. 150:2000;145-154.
20. Floyd S., De Camilli P. Endocytosis proteins and cancer. a potential link Trends Cell Biol. 8:1998;299-301.
21. Freije J.M., Blay P., MacDonald N.J., Manrow R.E., Steeg P.S. Site-directed mutation of Nm23-H1. Mutations lacking motility suppressive capacity upon transfection are deficient in histidine-dependent protein phosphotransferase pathways in vitro. J. Biol. Chem. 272:1997;5525-5532.
22. Fukuda M., Ishii A., Yasutomo Y., Shimada N., Ishikawa N., Hanai N., Nagata N., Irimura T., Nicolson G.L., Kimura N. Decreased expression of nucleoside diphosphate kinase alpha isoform, an nm23-H2 gene homolog, is associated with metastatic potential of rat mammary-adenocarcinoma cells. Int. J. Cancer. 65:1996;531-537.
23. Futter C.E., Pearse A., Hewlett L.J., Hopkins C.R. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132:1996;1011-1023.
24. Gonzalez-Gaitan M., Jackle H. Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell. 88:1997;767-776.
25. Grant D., Unadkat S., Katzen A., Krishnan K.S., Ramaswami M. Probable mechanisms underlying interallelic complementation and temperature-sensitivity of mutations at the shibire locus of Drosophila melanogaster. Genetics. 149:1998;1019-1030.
26. Jongeward G.D., Clandinin T.R., Sternberg P.W. sli-1, a negative regulator of let-23-mediated signaling in C. elegans. Genetics. 139:1995;1553-1566.
27. Kantor J.D., McCormick B., Steeg P.S., Zetter B.R. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res. 53:1993;1971-1973.
28. Kelly L.E., Suzuki D.T. The effects of increased temperature on electroretinograms of temperature-sensitive paralysis mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 71:1974;4906-4909.
29. Kim Y.-T., Wu C.-F. Allelic interactions at the shibire locus of Drosophila. effects on behaviour J. Neurogenet. 7:1990;1-14.
30. Koenig J., Ikeda K. Disappearance and reappearance of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9:1989;3844-3860.
31. Koenig J.H., Ikeda K. Synaptic vesicles have two distinct recycling pathways. J. Cell Biol. 135:1996;797-808.
32. Koenig J.H., Ikeda K. Contribution of active zone subpopulation of vesicles to evoked and spontaneous release. J. Neurophysiol. 81:1999;1495-1505.
33. Kosaka T., Ikeda K. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14:1983;207-225.
34. Kramer H., Cagan R.L., Zipursky S.L. Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature. 352:1991;207-212.
35. ts mutants in Drosophila by subanesthetic concentrations of carbon dioxide. J. Neurogenet. 10:1996;221-238.
36. Lascu I., Chaffotte A., Limbourg-Bouchon B., Veron M. A Pro/Ser substitution in nucleoside diphosphate kinase of Drosophila melanogaster (mutation killer of prune) affects stability but not catalytic efficiency of the enzyme. J. Biol. Chem. 267:1992;12775-12781.
37. Leone A., Flatow U., King C.R., Sandeen M.A., Margulies I.M., Liotta L.A., Steeg P.S. Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23-transfected melanoma cells. Cell. 65:1991;25-35.
38. Leone A., Flatow U., VanHoutte K., Steeg P.S. Transfection of human nm23-H1 into the human MDA-MB-435 breast carcinoma cell line. effects on tumor metastatic potential, colonization and enzymatic activity Oncogene. 8:1993;2325-2353.
39. Levkowitz G., Waterman H., Zamir E., Kam Z., Oved S., Langdon W.Y., Beguinot L., Geiger B., Yarden Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12:1998;3663-3674.
40. Levkowitz G., Waterman H., Ettenberg S.A., Katz M., Tsygankov A.Y., Alroy I., Lavi S., Iwai K., Reiss Y., Ciechanover A.et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell. 4:1999;1029-1040.
41. Loughney K., Kreber R., Ganetzky B. Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell. 58:1989;1143-1154.
42. MacDonald N.J., Freije J.M.P., Stracke M.L., Manrow R.E., Steeg P.S. Site-directed mutagenesis of nm23-H1. Mutation of proline 96 or serine 120 abrogates its motility inhibitory activity upon transfection into human breast carcinoma cells. J. Biol. Chem. 271:1996;25107-25116.
43. Marsh M., McMahon H.T. The structural era of endocytosis. Science. 285:1999;215-220.
44. McNiven M.A., Cao H., Pitts K.R., Yoon Y. The dynamin family of mechanozymes. pinching in new places Trends Biochem. Sci. 25:2000;115-120.
45. Pallanck L., Ordway R.W., Ganetzky B. A Drosophila NSF mutant. Nature. 376:1995;25.
46. Parhar R.S., Shi Y., Zou M., Farid N.R., Ernst P., al-Sedairy S.T. Effects of cytokine-mediated modulation of nm23 expression on the invasion and metastatic behavior of B16F10 melanoma cells. Int. J. Cancer. 60:1995;204-210.
47. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron. 19:1997;1237-1248.
48. Poodry C.A. shibire. a neurogenic mutant of Drosophila Dev. Biol. 138:1990;464-472.
49. Poodry C.A., Edgar L. Reversible alterations in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J. Cell. Biol. 81:1979;520-527.
50. Ramaswami M., Rao S., van der Bliek A., Kelly R.B., Krishnan K.S. Genetic studies on dynamin function in Drosophila. J. Neurogenet. 9:1993;73-87.
51. Ramaswami M., Krishnan K.S., Kelly R.B. Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron. 13:1994;363-375.
52. Randazzo P.A., Kahn R.A., Northup J.K. Nucleoside diphosphate kinase. conclusions withdrawn Science. 257:1992;862.
53. Richter M.F., Schwemmle M., Herrmann C., Wittinghofer A., Staeheli P. Interferon-induced MxA protein. GTP binding and GTP hydrolysis properties. J. Biol. Chem. 270:1995;13512-13517.
54. Roos J., Kelly R.B. Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem. 273:1998;19108-19119.
55. Roos J., Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9:1999;1411-1414.
56. Rosengard A.M., Krutzsch H.C., Shearn A., Biggs J.R., Barker E., Margulies I.M., King C.R., Liotta L.A., Steeg P.S. Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development. Nature. 342:1989;177-180.
57. Sever S., Muhlberg A.B., Schmid S.L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature. 398:1999;481-486.
58. Sever S., Damke H., Schmid S.L. Garrotes, springs, ratchets and whips. putting dynamin models to the test Traffic. 1:2000;385-392. a.
59. Sever S., Damke H., Schmid S.L. Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell Biol. 50:2000;1137-1148. b.
60. Shpetner H., Vallee R. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell. 59:1989;421-432.
61. Shpetner H.S., Vallee R.B. Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature. 355:1992;733-735.
62. Simon M.A., Bowtell D.D., Dodson G.S., Laverty T.R., Rubin G.M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 67:1991;701-716.
63. Steeg P.S., Bevilacqua G., Kopper L., Thorgeirsson U.P., Talmadge J.E., Liotta L.A., Sobel M.E. Evidence for a novel gene associated with low tumor metastatic potential. J. Natl. Cancer Inst. 80:1988;200-204. a.
64. Steeg P.S., Bevilacqua G., Pozzatti R., Liotta L.A., Sobel M.E. Altered expression of NM23, a gene associated with low tumor metastatic potential, during adenovirus 2 Ela inhibition of experimental metastasis. Cancer Res. 48:1988;6550-6554. b.
65. Stimson D.T., Estes P.S., Smith M., Kelly L.E., Ramaswami M. A product of the Drosophila stoned locus regulates neurotransmitter release. J. Neurosci. 18:1998;9638-9649.
66. Sturtevant A.H. Genetics. 41:1956;118-123.
67. Takei K., McPherson P.S., Schmid S., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTPgS in nerve terminals. Nature. 374:1995;186-190.
68. Teng D.H., Engele C.M., Venkatesh T.R. A product of the prune locus of Drosophila is similar to mammalian GTPase-activating protein. Nature. 353:1991;437-440.
69. Timmons L., Hersperger E., Woodhouse E., Xu J., Liu L.Z., Shearn A. The expression of the Drosophila awd gene during normal development and in neoplastic brain tumors caused by lgl mutations. Dev. Biol. 158:1993;364-379.
70. Timmons L., Xu J., Hersperger G., Deng X.F., Shearn A. Point mutations in awdKpn which revert the prune/Killer of prune lethal interaction affect conserved residues that are involved in nucleoside diphosphate kinase substrate binding and catalysis. J. Biol. Chem. 270:1995;23021-23030.
71. van der Bliek A. Functional diversity in the dynamin family. Trends Cell Biol. 9:1999;96-102.
72. van der Bliek A., Meyerowitz E. Dynamin like protein encoded by the Drosophila shibire gene associated with membrane traffic. Nature. 351:1991;411-414.
73. ts1 mutant Drosophila. Proc. Natl. Acad. Sci. USA. 92:1995;5739-5743.
74. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:1996;2086-2089.
75. Wagner P.D., Steeg P.S., Vu N.D. Two-component kinase-like activity of nm23 correlates with its motility-suppressing activity. Proc. Natl. Acad. Sci. USA. 94:1997;9000-9005.
76. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron. 26:2000;313-329.
77. Warnock D.E., Schmid S.L. Dynamin GTPase, a force-generating molecular switch. Bioessays. 18:1996;885-893.
78. Whistler J.L., von Zastrow M. Dissociation of funtional roles of dynamin in receptor-mediated endocytosis and mitogen signal transduction. J. Biol. Chem. 274:1999;24575-24578.
79. Wu C.F., Wong F. Frequency characteristics in the visual system of Drosophila. genetic dissection of electroretinogram components J. Gen. Physiol. 69:1977;705-724.
80. Xu J., Liu L.Z., Deng X.F., Timmons L., Hersperger E., Steeg P.S., Veron M., Shearn A. The enzymatic activity of Drosophila AWD/NDP kinase is necessary but not sufficient for its biological function. Dev. Biol. 177:1996;544-557.
81. Yoon C.H., Lee J., Jongeward G.D., Sternberg P.W. Similarity of sli-1, a regulator of vulval development in C. elegans, to the mammalian proto-oncogene c-cbl. Science. 269:1995;1102-1105.
82. Zhu J., Tseng Y.H., Kantor J.D., Rhodes C.J., Zetter B.R., Moyers J.S., Kahn C.R. Interaction of the Ras-related protein associated with diabetes rad and the putative tumor metastasis suppressor NM23 provides a novel mechanism of GTPase regulation. Proc. Natl. Acad. Sci. USA. 96:1999;14911-14918.
83. Zuker C.S. The biology of vision of Drosophila. Proc. Natl. Acad. Sci. USA. 93:1996;571-576.