A Drosophila temperature-sensitive seizure mutant in phosphoglycerate kinase disrupts ATP generation and alters synaptic function

Journal of Neuroscience

Volumn 24, Issue 19, 2004, Pages 4518-4529

  Wang, Ping ^a   Saraswati, Sudipta ^a   Guan, Zhuo ^a   Watkins, Carol J ^a   Wurtman, Richard J ^a   Littleton, J Troy ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Drosophila; Endocytosis; Epilepsy; Glycolysis; Microarray; Seizure; Synaptic transmission

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BRAIN EXTRACT; GUANOSINE TRIPHOSPHATASE; MUTANT PROTEIN; PHOSPHOGLYCERATE KINASE;

ARTICLE; BEHAVIOR; CELL ACTIVITY; CHEMICAL ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME DEFICIENCY; EPILEPSY; EXERCISE; EXOCYTOSIS; GLYCOLYSIS; LIFESPAN; LOCOMOTION; MENTAL DEFICIENCY; METABOLISM; MICROANALYSIS; NERVE CELL; NEUROPATHOLOGY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PARALYSIS; PARAMETER; PRIORITY JOURNAL; REGULATORY MECHANISM; SCREENING; SEIZURE; SYNAPTIC TRANSMISSION; TEMPERATURE SENSITIVITY; VARICOSIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BEHAVIOR, ANIMAL; CHROMOSOME MAPPING; DROSOPHILA; ELECTROPHYSIOLOGY; ENDOCYTOSIS; FEMALE; GENETIC SCREENING; LARVA; MALE; MEMBRANE PROTEINS; MUTAGENESIS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARALYSIS; PHOSPHOGLYCERATE KINASE; SEIZURES; SNARE PROTEINS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TEMPERATURE; VESICULAR TRANSPORT PROTEINS;

EID: 2442649103     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0542-04.2004     Document Type: Article

References (65)

1. Akasu T, Tsurusaki M, Shoji S (1996) Depletion of glucose causes presynaptic inhibition of neuronal transmission in the rat dorsolateral septal nucleus. Synapse 24:125-134.
2. Andrews J, Smith M, Merakovsky J, Coulson M, Hannan F, Kelly LE (1996) The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides. Genetics 143:1699-1711.
3. Atkinson NS, Robertson GA, Ganetzky B (1991) A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253:551-555.
4. Bernstein BE, Michels PA, Hol WG (1997) Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature 385:275-278.
5. Davis GW, Bezprozvanny I (2001) Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63:847-869.
6. Deary IJ, Sommerfield AJ, McAulay V, Frier BM (2003) Moderate hypoglycaemia obliterates working memory in humans with and without insulin-treated diabetes. J Neurol Neurosurg Psychiatry 74:278-279.
7. Delgado R, Maureira C, Oliva C, Kidokoro Y, Labarca P (2000) Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28:941-953.
8. DiMauro S, Dalakas M, Miranda AF (1983) Phosphoglycerate kinase deficiency: another cause of recurrent myoglobinuria. Ann Neurol 13:11-19.
9. Ganetzky B, Wu CF (1986) Neurogenetics of membrane excitability in Drosophila. Annu Rev Genet 20:13-44.
10. Gardiner RM (1999) Genetic basis of the human epilepsies. Epilepsy Res 36:91-95.
11. Hell JW, Maycox PR, Jahn R (1990) Energy dependence and functional reconstitution of the γ-aminobutyric acid carrier from synaptic vesicles. J Biol Chem 265:2111-2117.
12. Hoeffer CA, Sanyal S, Ramaswami M (2003) Acute induction of conserved synaptic signaling pathways in Drosophila melanogaster. J Neurosci 23:6362-6372.
13. Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 38:273-291.
14. Hotta Y, Benzer S (1969) Abnormal electroretinograms in visual mutants of Drosophila. Nature 222:354-356.
15. Ikemoto A, Bole DG, Ueda T (2003) Glycolysis and glutamate accumulation into synaptic vesicles. Role of glyceraldehyde phosphate dehydrogenase and 3-phosphoglycerate kinase. J Biol Chem 278:5929-5940.
16. Joiner MA, Griffith LC (1999) Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn Mem 6:177-192.
17. Katz B (1969) The release of neural transmitter substances. Liverpool, UK: Liverpool UP.
18. Kawasaki F, Mattiuz AM, Ordway RW (1998) Synaptic physiology and ultrastructure in comatose mutants define an in vivo role for NSF in neurotransmitter release. J Neurosci 18:10241-10249.
19. Kawasaki F, Felling R, Ordway RW (2000) A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J Neurosci 20:4885-4889.
20. Koenig JH, Ikeda K (1996) Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135:797-808.
21. Krishnan KS, Chakravarty S, Rao S, Raghuram V, Ramaswami M (1996) Alleviation of the temperature-sensitive paralytic phenotype of shibire(ts) mutants in Drosophila by sub-anesthetic concentrations of carbon dioxide. J Neurogenet 10:221-238.
22. Kuebler D, Zhang H, Ren X, Tanouye MA (2001) Genetic suppression of seizure susceptibility in Drosophila. J Neurophysiol 86:1211-1225.
23. Lewis EB, Bacher F (1968) Mutagenesis with ethyl methane-sulfonate. Dros Inf Serv 43:193.
24. Littleton JT, Bellen HJ (1994) Genetic and phenotypic analysis of 13 essential genes in cytological interval 22F1-2; 23B1-2 reveals novel genes required for neuronal development in Drosophila. Genetics 138:111-123.
25. Littleton JT, Bellen HJ, Perin M (1993) Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118:1077-1088.
26. Littleton JT, Chapman ER, Kreber R, Garment MB, Carlson SD, Ganetzky B (1998) Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron 21:401-413.
27. Littleton JT, Barnard RJ, Titus SA, Slind J, Chapman ER, Ganetzky B (2001) SNARE complex disassembly by NSF follows synaptic vesicle fusion. Proc Natl Acad Sci USA 98:12233-12238.
28. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261-269.
29. Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143-1154.
30. Maycox PR, Deckwerth T, Hell JW, Jahn R (1988) Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J Biol Chem 263:15423-15428.
31. McNay EC, Fries TM, Gold PE (2000) Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc Natl Acad Sci USA 97:2881-2885.
32. Pak WL, Grossfield J, White NV (1969) Nonphototactic mutants in a study of vision in Drosophila. Nature 222:351-354.
33. Pennetta G, Hiesinger P, Fabian-Fine R, Meinertzhagen I, Bellen HJ (2002) Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 35:291-306.
34. Perlmuter LC, Hakami MK, Hodgson-Harrington C, Ginsberg J, Katz J, Singer DE, Nathan DM (1984) Decreased cognitive function in aging non-insulin-dependent diabetic patients. Am J Med 77:1043-1048.
35. Puranam RS, McNamara JO (1999) Seizure disorders in mutant mice: relevance to human epilepsies. Curr Opin Neurobiol 9:281-287.
36. Rao SS, Stewart BA, Rivlin PK, Vilinsky I, Watson BO, Lang C, Boulianne G, Salpeter MM, Deitcher DL (2001) Two distinct effects on neurotransmission in a temperature-sensitive SNAP-25 mutant. EMBO J 20:6761-6771.
37. Reickhof GE, Yoshihara M, Guan Z, Littleton JT (2003) Presynaptic N-type calcium channels regulate synaptic growth. J Biol Chem 278:41099-41108.
38. Richards S, Hillman T, Stern M (1996) Mutations in the Drosophila pushover gene confer increased neuronal excitability and spontaneous synaptic vesicle fusion. Genetics 142:1215-1223.
39. Richardson JT (1990) Cognitive function in diabetes mellitus. Neurosci Biobehav Rev 14:385-388.
40. Rikhy R, Ramaswami M, Krishnan KS (2003) A temperature-sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 165:1243-1253.
41. Rogina B, Helfand SL, Frankel S (2002) Longevity regulation by Drosophila Rpd3 deacetylase and caloric restriction. Science 298:1745.
42. Saraswati S, Fox LE, Soll DR, Wu CF (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58:425-441.
43. Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3→CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300-8310.
44. Shoji S (1992) Glucose regulation of synaptic transmission in the dorsolateral septal nucleus of the rat. Synapse 12:322-332.
45. Siddiqi O, Benzer S (1976) Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 73:3253-3257.
46. Simmonds HA, Fairbanks LD, Morris GS, Webster DR, Harley EH (1988) Altered erythrocyte nucleotide patterns are characteristic of inherited disorders of purine or pyrimidine metabolism. Clin Chim Acta 171:197-210.
47. Soll DR (1995) The use of computers in understanding how animal cells crawl. Int Rev Cytol 163:43-103.
48. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324.
49. Sommerfield AJ, Deary IJ, McAulay V, Frier BM (2003) Moderate hypoglycemia impairs multiple memory functions in healthy adults. Neuropsychology 17:125-132.
50. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol [A] 175:179-191.
51. Suster ML, Bate M (2002) Embryonic assembly of a central pattern generator without sensory input. Nature 416:174-178.
52. ts) causing reversible adult paralysis. Proc Natl Acad Sci USA 68:890-893.
53. Tabb JS, Kish PE, Van Dyke R, Ueda T (1992) Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesicular pH. J Biol Chem 267:15412-15418.
54. Tein I (1996) Metabolic myopathies. Semin Pediatr Neurol 3:59-98.
55. + channel polypeptide is encoded by the seizure locus. J Neurosci 17:875-881.
56. Tolar LA, Pallanck L (1998) NSF function in neurotransmitter release involves rearrangement of the SNARE complex downstream of synaptic vesicle docking. J Neurosci 18:10250-10256.
57. Tsujino S, Shanske S, DiMauro S (1995) Molecular genetic heterogeneity of phosphoglycerate kinase (PGK) deficiency. Muscle Nerve 3:S45-S49.
58. Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221-227.
59. Vanhanen M, Koivisto K, Karjalainen L, Helkala EL, Laakso M, Soininen H, Riekkinen P (1997) Risk for non-insulin-dependent diabetes in the normoglycaemic elderly is associated with impaired cognitive function. NeuroReport 8:1527-1530.
60. + channel mutants revealed by computer-assisted motion analysis. J Neurogenet 11:231-254.
61. + channel mutants. J Neurogenet 16:45-63.
62. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Söllner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759-772.
63. + channels in isolated guinea pig cardiac myocytes. Science 238:67-69.
64. Yuan LL, Ganetzky B (1999) A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. Science 283:1343-1345.
65. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S (1994) Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263:977-980.