Tolerance to anesthesia depends on synaptic proteins

Behavior Genetics

Volumn 41, Issue 5, 2011, Pages 734-745

  Al Hasan, Yazan M ^a   Krishnan, Harish R ^a   Ghezzi, Alfredo ^a   Prado III, Francisco J ^a   Robles, Roseanna B ^a   Atkinson, Nigel S ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Anesthetic; Behavior; Benzyl alcohol; Drosophila; Drug abuse; N Ethylmaleimide; Paralytic; Shibire; Synapse; Tolerance

Indexed keywords

BENZYL ALCOHOL; CELL PROTEIN; DYNAMIN; N ETHYLMALEIMIDE; SYNAPTIC PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CELL VACUOLE; CLIMBING; CONTROLLED STUDY; DROSOPHILA; DRUG TOLERABILITY; DRUG TOLERANCE; DYNAMIN GENE; FEMALE; GENE; GENE MUTATION; GENETIC MANIPULATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; SEDATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC FUNCTION; TEMPERATURE SENSITIVITY;

ANESTHESIA; ANESTHESIOLOGY; ANESTHETICS; ANIMALS; BENZYL ALCOHOL; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DRUG TOLERANCE; ELECTROPHYSIOLOGY; ETHYLMALEIMIDE; MUTATION; NEURONS; SIGNAL TRANSDUCTION; SUBSTANCE-RELATED DISORDERS; SYNAPSES; SYNAPTIC VESICLES; TEMPERATURE; TIME FACTORS;

EID: 80054860749     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-011-9451-8     Document Type: Article

References (55)

1. Atkinson NS (2009) Tolerance in Drosophila. J Neurogenet 23:293-302
2. Barrantes FJ (1993) Structural-functional correlates of the nicotinic acetylcholine receptor and its lipid microenvironment. FASEB J 7:1460-1467 (Pubitemid 24003265)
3. Berger KH, Kong EC, Dubnau J, Tully T, Moore MS, Heberlein U (2008) Ethanol sensitivity and tolerance in long-term memory mutants of Drosophila melanogaster. Alcohol Clin Exp Res 32:895-908 (Pubitemid 351589401)
4. Block MR, Glick BS, Wilcox CA, Wieland FT, Rothman JE (1988) Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci USA 85:7852-7856
5. Chalon J, Tang CK, Roberts C, Walpert L, Hoffman C, Ramanathan S, Turndorf H (1983) Murine auto-and cross-tolerance to volatile anaesthetics. Can Anaesth Soc J 30:230-234 (Pubitemid 13100407)
6. Chao J, Nestler EJ (2004) Molecular neurobiology of drug addiction. Annu Rev Med 55:113-132 (Pubitemid 38316718)
7. Chen ML, Green D, Liu L, Lam YC, Mukai L, Rao S, Ramagiri S, Krishnan KS, Engel JE, Lin JJ, Wu CF (2002) Unique biochemical and behavioral alterations in Drosophila shibire(ts1) mutants imply a conformational state affecting dynamin subcellular distribution and synaptic vesicle cycling. J Neurobiol 53:319-329 (Pubitemid 35231793)
8. Cowmeadow RB, Krishnan HR, Atkinson NS (2005) The slowpoke gene underlies rapid ethanol tolerance in Drosophila. Alcohol Clin Exp Res 29:1777-1786 (Pubitemid 41579127)
9. Cowmeadow RB, Krishnan HR, Ghezzi A, Al'hasan Y, Wang YZ, Atkinson NS (2006) Ethanol tolerance caused by slowpoke induction in Drosophila. Alcohol Clin Exp Res 30:745-753
10. Davis GW (2006) Homeostatic control of neural activity: From phenomenology to molecular design. Annu Rev Neurosci 29:307-323 (Pubitemid 44476848)
11. Dzitoyeva S, Dimitrijevic N, Manev H (2003) Gamma-aminobutyric acid B receptor 1 mediates behavior-impairing actions of alcohol in Drosophila: Adult RNA interference and pharmacological evidence. Proc Natl Acad Sci USA 100:5485-5490 (Pubitemid 36542731)
12. Edgecomb RS, Harth CE, Schneiderman AM (1994) Regulation of feeding behavior in adult Drosophila melanogaster varies with feeding regime and nutritional state. J Exp Biol 197:215-235
13. Elkins T, Ganetzky B (1990) Conduction in the giant nerve fiber pathway in temperature-sensitive paralytic mutants of Drosophila. J Neurogenet 6:207-219
14. Futterer CD, Maurer MH, Schmitt A, Feldmann REJ, Kuschinsky W, Waschke KF (2004) Alterations in rat brain proteins after desflurane anesthesia. Anesthesiology 100:302-308 (Pubitemid 38133697)
15. Gamo S, Ogaki M, Nakashima-Tanaka E (1981) Strain differences in minimum anesthetic concentrations in Drosophila melanogaster. Anesthesiology 54:289-293 (Pubitemid 11147387)
16. Ganetzky B (2000) Genetic analysis of ion channel dysfunction in Drosophila. Kidney Int 57:766-771 (Pubitemid 30434764)
17. Ghezzi A, Al-Hasan YM, Larios LE, Bohm RA, Atkinson NS (2004) slo K? channel gene regulation mediates rapid drug tolerance. Proc Natl Acad Sci USA 101:17276-17281 (Pubitemid 39627810)
18. Ghezzi A, Pohl JB, Wang Y, Atkinson NS (2010) BK channels play a counteradaptive role in drug tolerance and dependence. Proc Natl Acad Sci USA 107:16360-16365
19. Godenschwege TA, Reisch D, Diegelmann S, Eberle K, Funk N, Heisenberg M, Hoppe V, Hoppe J, Klagges BR, Martin JR, Nikitina EA, Putz G, Reifegerste R, Reisch N, Rister J, Schaupp M, Scholz H, Schwarzel M, Werner U, Zars TD, Buchner S, Buchner E (2004) Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 20:611-622 (Pubitemid 39036925)
20. Gorini G, Ponomareva O, Shores KS, Person MD, Harris RA, Mayfield RD (2010) Dynamin-1 co-associates with native mouse brain BKCa channels: Proteomics analysis of synaptic protein complexes. FEBS Lett 584:845-851
21. Grigliatti TA, Hall L, Rosenbluth R, Suzuki DT (1973) Temperaturesensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults. Mol Gen Genet 120:107-114
22. Haeseler G, Mamarvar M, Bufler J, Dengler R, Hecker H, Aronson JK, Piepenbrock S, Leuwer M (2000) Voltage-dependent blockade of normal and mutant muscle sodium channels by benzylalcohol. Br J Pharmacol 130:1321-1330 (Pubitemid 30488596)
23. Hemmings HCJ (2009) Sodium channels and the synaptic mechanisms of inhaled anaesthetics. Br J Anaesth 103:61-69
24. Herring BE, Xie Z, Marks J, Fox AP (2009) Isoflurane inhibits the neurotransmitter release machinery. J Neurophysiol 102: 1265-1273
25. Hummon MR, Costello WJ (1989) Giant fiber activation of flight muscles in Drosophila: Asynchrony in latency of wing depressor fibers. J Neurobiol 20:593-602
26. Humphrey JA, Hamming KS, Thacker CM, Scott RL, Sedensky MM, Snutch TP, Morgan PG, Nash HA (2007) A putative cation channel and its novel regulator: Cross-species conservation of effects on general anesthesia. Curr Biol 17:624-629 (Pubitemid 46497797)
27. Kalant H (1998) Research on tolerance: What can we learn from history? Alcohol Clin Exp Res 22:67-76 (Pubitemid 28139197)
28. Kalenka A, Hinkelbein J, Feldmann REJ, Kuschinsky W, Waschke KF, Maurer MH (2007) The effects of sevoflurane anesthesia on rat brain proteins: A proteomic time-course analysis. Anesth Analg 104:1129-1135 (Pubitemid 46649933)
29. Kelly LE, Suzuki DT (1974) The effects of increased temperature on electroretinograms of temperature-sensitive paralysis mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 71: 4906-4909
30. Koenig JH, Saito K, Ikeda K (1983) Reversible control of synaptic transmission in a single gene mutant of Drosophila melanogaster. J Cell Biol 96:1517-1522 (Pubitemid 13034426)
31. Kosaka T, Ikeda K (1983) Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurobiol 14:207-225 (Pubitemid 13058761)
32. Kulkarni NH, Yamamoto AH, Robinson KO, Mackay TF, Anholt RR (2002) The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics 161:1507-1516 (Pubitemid 35014752)
33. Lesch KP (2005) Alcohol dependence and gene 9 environment interaction in emotion regulation: Is serotonin the link? Eur J Pharmacol 526:113-124
34. Lin WH, Wright DE, Muraro NI, Baines RA (2009) Alternative splicing in the voltage-gated sodium channel DmNav regulates activation, inactivation, and persistent current. J Neurophysiol 102:1994-2006
35. 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 (Pubitemid 28399700)
36. Lledo PM, Zhang X, Sudhof TC, Malenka RC, Nicoll RA (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279:399-403 (Pubitemid 28063378)
37. Markham MR, McAnelly ML, Stoddard PK, Zakon HH (2009) Circadian and social cues regulate ion channel trafficking. PLoS Biol 7:e1000203
38. Moore MS, DeZazzo J, Luk AY, Tully T, Singh CM, Heberlein U (1998) Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93:997-1007 (Pubitemid 28280793)
39. Nelson JC, Wyman RJ (1990) Examination of paralysis in Drosophila temperature-sensitive paralytic mutations affecting sodium channels; a proposed mechanism of paralysis. J Neurobiol 21:453-469 (Pubitemid 20155931)
40. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12:1934-1940 (Pubitemid 35426707)
41. Pittson S, Himmel AM, MacIver MB (2004) Multiple synaptic and membrane sites of anesthetic action in the CA1 region of rat hippocampal slices. BMC Neurosci 5:52
42. Ramazani RB, Krishnan HR, Bergeson SE, Atkinson NS (2007) Computer automated movement detection for the analysis of behavior. J Neurosci Methods 162:171-179 (Pubitemid 46527923)
43. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28:261-271
44. Scholz H, Franz M, Heberlein U (2005) The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436:845-847 (Pubitemid 41160642)
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. Smith RA, Winter PM, Smith M, Eger EI (1979) Tolerance to and dependence on inhalational anesthetics. Anesthesiology 50: 505-509 (Pubitemid 9239492)
47. Staiman A, Seeman P (1977) Conduction-blocking concentrations of anesthetics increase with nerve axon diameter: Studies with alcohol, lidocaine and tetrodotoxin on single myelinated fibers. J Pharmacol Exp Ther 201:340-349
48. Suzuki DT, Grigliatti T, Williamson R (1971) Temperature sensitive mutations in Drosophila melanogaster. VII. A mutations (parats1) causing reversible adult paralysis. Proc Natl Acad Sci USA 68:890-893
49. Takadera T, Ohyashiki T (2008) Benzyl alcohol inhibits N-methyl-Daspartate receptor-mediated neurotoxicity and calcium accumulation in cultured rat cortical neurons. J Biomed Sci 15:767-770
50. 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 (Pubitemid 29016544)
51. Urizar NL, Yang Z, Edenberg HJ, Davis RL (2007) Drosophila homer is required in a small set of neurons including the ellipsoid body for normal ethanol sensitivity and tolerance. J Neurosci 27: 4541-4551 (Pubitemid 46663562)
52. van Swinderen B, Greenspan RJ (2003) Salience modulates 20-30 Hz brain activity in Drosophila. Nat Neurosci 6:579-586 (Pubitemid 36648798)
53. Walcourt A, Scott RL, Nash HA (2001) Blockage of one class of potassium channel alters the effectiveness of halothane in a brain circuit of Drosophila. Anesth Analg 92:535-541 (Pubitemid 32127649)
54. Wang Y, Krishnan HR, Ghezzi A, Yin JC, Atkinson NS (2007) Druginduced epigenetic changes produce drug tolerance. PLoS Biol 5:2342-2353 (Pubitemid 350035433)
55. Wang Y, Ghezzi A, Yin JC, Atkinson NS (2009) CREB regulation of BK channel gene expression underlies rapid drug tolerance. Genes Brain Behav 8:369-376