Equilibrative nucleoside transporter 2 regulates associative learning and synaptic function in Drosophila

Journal of Neuroscience

Volumn 30, Issue 14, 2010, Pages 5047-5057

  Knight, David ^a   Harvey, Philip J ^a   Iliadi, Konstantin G ^a   Klose, Markus K ^a   Iliadi, Natalia ^a   Dolezelova, Eva ^b   Charlton, Milton P ^c   Zurovec, Michal ^b   Boulianne, Gabrielle L ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE RECEPTOR; CALCIUM; NUCLEOTIDE TRANSPORTER; NUCLEOTIDE TRANSPORTER 2; RNA; UNCLASSIFIED DRUG;

ALLELE; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CALCIUM TRANSPORT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; EXCITATORY JUNCTION POTENTIAL; LARVAL STAGE; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; STATE DEPENDENT LEARNING; SYNAPTIC TRANSMISSION;

ANIMALS; ASSOCIATION LEARNING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MEMBRANE TRANSPORT PROTEINS; SYNAPSES;

EID: 77950613028     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6241-09.2010     Document Type: Article

References (55)

1. Ackley MA, Governo RJ, Cass CE, Young JD, Baldwin SA, King AE (2003) Control of glutamatergic neurotransmission in the rat spinal dorsal horn by the nucleoside transporter ENT1. J Physiol 548:507-517.
2. Alanko L, Stenberg D, Porkka-Heiskanen T (2003) Nitrobenzylthioinosine (NBMPR) binding and nucleoside transporter ENT1 mRNA expression after prolonged wakefulness and recovery sleep in the cortex and basal forebrain of rat. J Sleep Res 12:299-304.
3. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, Ito K, Hama C (2000) The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26:119-131.
4. Berry J, Krause WC, Davis RL (2008) Olfactory memory traces in Drosophila. Prog Brain Res 169:293-304.
5. Bragina YV, Kamyshev NG (2003) Comparative studies of four Drosophila P-insertion mutants with memory defects. Neurosci Behav Physiol 33:73-79.
6. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
7. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7:575-590.
8. Chen J, Rinaldo L, Lim SJ, Young H, Messing RO, Choi DS (2007) The type 1 equilibrative nucleoside transporter regulates anxiety-like behavior in mice. Genes Brain Behav 6:776-783.
9. Cheung U, Atwood HL, Zucker RS (2006) Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J Neurobiol 66:273-280.
10. Cheung US, Shayan AJ, Boulianne GL, Atwood HL (1999) Drosophila larval neuromuscular junction's responses to reduction of cAMP in the nervous system. J Neurobiol 40:1-13.
11. Choi DS, Cascini MG, Mailliard W, Young H, Paredes P, McMahon T, Diamond I, Bonci A, Messing RO (2004) The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nat Neurosci 7:855-861.
12. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
13. Del Castillo J, Katz B (1954) Quantal componentsofthe end-plate potential. J Physiol 124:560-573.
14. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156.
15. Dolezal T, Dolezelova E, Zurovec M, Bryant PJ (2005) A role for adenosine deaminase in Drosophila larval development. PLoS Biol 3: e201.
16. Dolezelova E, Nothacker HP, Civelli O, Bryant PJ, Zurovec M (2007) A Drosophila adenosine receptor activates cAMP and calcium signaling. Insect Biochem Mol Biol 37:318-329.
17. Downie MJ, Kirk K, Mamoun CB (2008) Purine salvage pathways in the intraerythrocytic malaria parasite Plasmodium falciparum. Eukaryot Cell 7:1231-1237.
18. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol 117:109-128.
19. Feng Y, Ueda A, Wu CF (2004) A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet 18:377-402.
20. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811. (Pubitemid 28099681)
21. Fisher SA, Fischer TM, Carew TJ (1997) Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci 20:170-177.
22. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553.
23. Guillen-Gómez E, Calbet M, Casado J, de Lecea L, Soriano E, Pastor-Anglada M, Burgaya F (2004) Distribution of CNT2 and ENT1 transcripts in rat brain: selective decrease of CNT2 mRNA in the cerebral cortex of sleepdeprived rats. J Neurochem 90:883-893.
24. Han PL, Levin LR, Reed RR, Davis RL (1992) Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9:619-627.
25. Jan LY, Jan YN (1976) L-Glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 262:215-236.
26. Kamyshev NG, Iliadi KG, Bragina YV, Savvateeva-Popova EV, Tokmacheva EV, Preat T (2000) Identification of Drosophila mutant with memory defects after acquisition of conditioned reflex suppression of courtship. Neurosci Behav Physiol 30:307-313.
27. Karunanithi S, Marin L, Wong K, Atwood HL (2002) Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22:10267-10276.
28. Klose MK, Boulianne GL, Robertson RM, Atwood HL (2009) Role of ATP-dependent calcium regulation in modulation of Drosophila synaptic thermotolerance. J Neurophysiol 102:901-913.
29. Knight D, Iliadi K, Charlton MP, Atwood HL, Boulianne GL (2007) Presynaptic plasticity and associative learning are impaired in a Drosophila presenilin null mutant. Dev Neurobiol 67:1598-1613.
30. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53:103-115.
31. Kuromi H, Kidokoro Y (2000) Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27:133-143.
32. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
33. Lima SQ, Miesenbock G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141-152.
34. Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35-43.
35. Lnenicka GA, Grizzaffi J, Lee B, Rumpal N (2006) Ca2+ dynamics along identified synaptic terminals in Drosophila larvae. J Neurosci 26:12283-12293.
36. Machado J, Abdulla P, Hanna WJ, Hilliker AJ, Coe IR (2007) Genomic analysis of nucleoside transporters in Diptera and functional characterization of DmENT2, a Drosophila equilibrative nucleoside transporter. Physiol Genomics 28:337-347. (Pubitemid 46708773)
37. Macleod GT, Hegstrom-Wojtowicz M, Charlton MP, Atwood HL (2002) Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88:2659-2663.
38. Meester BJ, Shankley NP, Welsh NJ, Meijler FL, Black JW (1998) Pharmacological analysis of the activity of the adenosine uptake inhibitor, dipyridamole, on the sinoatrial and atrioventricular nodes of the guinea pig. Br J Pharmacol 124:729-741.
39. Molotova-Besedina NG, Iliadi NN, Bragina IV, Kamysheva EA, Soboleva SA, Iliadi KG, Kamyshev NG (2009) Novel memory mutants in Drosophila: behavioral characteristics of the P-insertional mutant in the Ent2P locus (in Russian). Genetika 45:50-58.
40. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861-872.
41. Nighorn A, Healy MJ, Davis RL (1991) The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6:455-467.
42. Pastor-Anglada M, Cano-Soldado P, Errasti-Murugarren E, Casado FJ (2008) SLC28 genes and concentrative nucleoside transporter (CNT) proteins. Xenobiotica 38:972-994.
43. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
44. Rose JB, Coe IR (2008) Physiology of nucleoside transporters: back to the future. Physiology (Bethesda) 23:41-48.
45. Sankar N, Machado J, Abdulla P, Hilliker AJ, Coe IR (2002) Comparative genomic analysis of equilibrative nucleoside transporters suggests conserved protein structure despite limited sequence identity. Nucleic Acids Res 30:4339-4350.
46. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 157:263-277.
47. Vautrin J, Barker JL (2003) Presynaptic quantal plasticity: Katz's original hypothesis revisited. Synapse 47:184-199.
48. Yoshihara M, Suzuki K, Kidokoro Y (2000) Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20:8315-8322.
49. Young JD, Yao SY, Sun L, Cass CE, Baldwin SA (2008) Human equilibrative nucleoside transporter (ENT) family of nucleoside and nucleobase transporter proteins. Xenobiotica 38:995-1021.
50. Zhang J, Visser F, King KM, Baldwin SA, Young JD, Cass CE (2007) The role of nucleoside transportersincancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev 26:85-110.
51. Zhao H, Zheng X, Yuan X, Wang L, Wang X, Zhong Y, Xie Z, Tully T (2009) ben functions with scamp during synaptic transmission and long-term memory formation in Drosophila. J Neurosci 29:414-424.
52. Zhong Y, Wu CF (1991) Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251:198-201.
53. Zhong Y, Budnik V, Wu CF (1992) Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J Neurosci 12:644-651.
54. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.
55. Zurovec M, Dolezal T, Gazi M, Pavlova E, Bryant PJ (2002) Adenosine deaminase-related growth factors stimulate cell proliferation in Drosophila by depleting extracellular adenosine. Proc Natl Acad Sci U S A 99:4403-4408.