Resistance to volatile anesthetics by mutations enhancing excitatory neurotransmitter release in Caenorhabditis elegans

Genetics

Volumn 168, Issue 2, 2004, Pages 831-843

  Hawasli, Ammar H ^a   Saifee, Owais ^a   Liu, Christine ^a   Nonet, Michael L ^a   Crowder, C Michael ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; HALOTHANE; INHALATION ANESTHETIC AGENT; NEUROTRANSMITTER; PHOSPHOTRANSFERASE; POTASSIUM CHANNEL; SYNTAXIN; SYNTAXIN 1A; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CAENORHABDITIS ELEGANS; EGL 30 GENE; GENE; GENE FUNCTION; GENE MUTATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SLO 1 GENE; UNC 43 GENE; UNC 64 GENE;

ANESTHETICS, INHALATION; ANIMALS; ANTIGENS, SURFACE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DRUG RESISTANCE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; NEUROTRANSMITTER AGENTS; PHENOTYPE; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; QA-SNARE PROTEINS; SUPPRESSION, GENETIC; SYNTAXIN 1;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; NEMATODA;

EID: 8544262156     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.030502     Document Type: Article

References (76)

1. AHMED, S., I. N. MARUYAMA, R. KOZMA, J. LEE, S. BRENNER et al., 1992 The Caenorhabditis elegans unc-13 gene product is a phospholipid-dependent high-affinity phorbol ester receptor. Biochem. J. 287: 995-999.
2. AVERY, L., 1993 The genetics of feeding in Caenarhabditis elegans. Genetics 133: 897-917.
3. BARNES, T., and S. HEKIMI, 1997 The Caenarhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J. Neurochem. 69: 2251-2260.
4. BETZ, A., U. ASHERY, M. RICKMANN, I. AUGUSTIN, E. NEHER et al., 1998 Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21: 123-136.
5. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
6. BROSE, N., C. ROSENMUND and J. RETTIG, 2000 Regulation of transmitter release by Unc-13 and its homologues. Curr. Opin. Neurobiol. 10: 303-311.
7. BRUNDAGE, L., L. AVERY, A. KATZ, U. J. KIM, J. E. MENDEL et al., 1996 Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16: 999-1009.
8. BRUNGER, A. T., and J. A. ERNST, 2002 High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex. J. Biol. Chem. 20: 20.
9. CHASE, D. L., G. A. PATIKOGLOU and M. R. KOELLE, 2001 Two RGS proteins that inhibit Galpha(o) and Galpha(q) signaling in C. elegans neurons require a Gbeta(5)-like subunit for function. Curr. Biol. 11: 222-231.
10. CHEN, Y. A., and R. H. SCHELLER, 2001 SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell. Biol. 2: 98-106.
11. CROWDER, C. M., L. D. SHEBESTER and T. SCHEDL, 1996 Behavioral effects of volatile anesthetics in Caenorhabditis elegans. Anesthesiology 85: 901-912.
12. DAVIES, A. G., J. T. PIERCE-SHIMOMURA, H. KIM, M. K. VANHOVEN, T. R. THIELE et al., 2003 A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 115: 655-666.
13. DELEAN, A., P. J. MUNSON and D. RODBARD, 1978 Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am. J. Physiol. 235: E97-E102.
14. DOI, M., and K. IWASAKI, 2002 Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33: 249-259.
15. FRANKS, N. P., and W. R. LIEB, 1994 Molecular and cellular mechanisms of general anaesthesia. Nature 367: 607-614.
16. GAMO, S., J. TOMIDA, K. DODO, D. KEYAKIDANI, H. MATAKATSU et al., 2003 Calreticulin mediates anesthetic sensitivity in Drosophila melanogaster. Anesthesiology 99: 867-875.
17. HAGHIGHI, A. P., B. D. McCABE, R. D. FETTER, J. E. PALMER, S. HOM et al., 2003 Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. Neuron 39: 255-267.
18. HAJDU-CRONIN, Y. M., W. J. CHEN, G. PATIKOGLOU, M. R. KOELLE and P. W. STERNBERG, 1999 Antagonism between G(o)alpha and G(q)alpha in Caenorhabditis elegans: the RGS protein EAT-16 is necessary for G(o)alpha signaling and regulates G(q)alpha activity. Genes Dev. 13: 1780-1793.
19. HONG, Y., E. PUIL and D. A. MATHERS, 1994 Effect of halothane on large-conductance calcium-dependent potassium channels in cerebrovascular smooth muscle cells of the rat. Anesthesiology 81: 649-656.
20. HUMPHREY, J. A., M. M. SEDENSKY and P. G. MORGAN, 2002 Understanding anesthesia: making genetic sense of the absence of senses. Hum. Mol. Genet. 11: 1241-1249.
21. JAHN, R., and T. C. SUDHOF, 1999 Membrane fusion and exocytosis. Annu. Rev. Biochem. 68: 863-911.
22. JONES, M. V., P. A. BROOKS and N. L. HARRISON, 1992 Enhancement of gamma-aminobutyric acid-activated Cl- currents in cultured rat hippocampal neurones by three volatile anaesthetics. J. Physiol. 449: 279-293.
23. JURD, R., M. ARRAS, S. LAMBERT, B. DREXLER, R. SIEGWART et al., 2003 General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit. FASEB J. 17: 250-252.
24. KRISHNAN, K. S., and H. A. NASH, 1990 A genetic study of the anesthetic response: mutants of Drosophila melanogaster altered in sensitivity to halothane. Proc. Natl. Acad. Sci. USA 87: 8632-8636.
25. KULLMANN, D. M., R. L. MARTIN and S. J. REDMAN, 1989 Reduction by general anaesthetics of group Ia excitatory postsynaptic potentials and currents in the cat spinal cord. J. Physiol. 412: 277-296.
26. LACKNER, M. R., S. J. NURRISH and J. M. KAPLAN, 1999 Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335-346.
27. LEIBOVITCH, B. A., D. B. CAMPBELL, K. S. KRISHNAN and H. A. NASH, 1995 Mutations that affect ion channels change the sensitivity of Drosophila melanogaster to volatile anesthetics.J. Neurogenet. 10: 1-13.
28. MACIVER, M. B., A. A. MIKULEC, S. M. AMAGASU and F. A. MONROE, 1996 Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 85: 823-834.
29. MARUYAMA, I. N., and S. BRENNER, 1991 A phorbol ester/diacylglycerol- binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 88: 5729-5733.
30. MCINTIRE, S. L., E. JORGENSEN and H. R. HORVITZ, 1993 Genes required for GABA function in Caenorhabditis elegans. Nature 364: 334-337.
31. MELLO, C., and A. FIRE, 1995 DNA transformation, pp. 451-482 in Caenorhabditis elegans: Modern Biological Analysis of an Organism, edited by H. EPSTEIN and D. SHAKES. Academic Press, San Diego.
32. 2+ transients and glutamate release in isolated cerebral synaptosomes. Anesthesiology 83: 593-603.
33. MIHIC, S. J., Q. YE, M. J. WICK, V. V. KOLTCHINE, M. D. KRASOWSKI et al., 1997 Sites of alcohol and volatile anaesthetic action on GABA(A) and glycine receptors Nature 389: 385-389.
34. MILLER, K. G., M. D. EMERSON and J. B. RAND, 1999 Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24: 323-333.
35. MOCHIDA, S., 2000 Protein-protein interactions in neurotransmitter release. Neurosci. Res. 36: 175-182.
36. MORGAN, P. G., and H. F. CASCORBI, 1985 Effect of anesthetics and a convulsant on normal and mutant Caenorhabditis elegans. Anesthesiology 62: 738-744.
37. MORGAN, P. G., and M. M. SEDENSKY, 1994 Mutations conferring new patterns of sensitivity to volatile anesthetics in Caenorhabditis elegans. Anesthesiology 81: 888-898.
38. MORGAN, P. G., M. M. SEDENSKY, P. M. MENEELY and H. F. CASCORBI, 1988 The effect of two genes on anesthetic response in the nematode Caenorhabditis elegans. Anesthesiology 69: 246-251.
39. MORGAN, P. G., M. SEDENSKY and P. M. MENEELY, 1990 Multiple sites of action of volatile anesthetics in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 87: 2965-2969.
40. NISHIKAWA, K., and Y. KIDOKORO, 1999 Halothane presynaptically depresses synaptic transmission in wild-type Drosophila larvae but not in halothane-resistant (har) mutants. Anesthesiology 90: 1691-1697.
41. NISHIKAWA, K.-I., and M. B. MACIVER, 2000 Excitatory synaptic transmission mediated by NMDA receptors is more sensitive to isoflurane than are non-NMDA receptor-mediated responses. Anesthesiology 92: 228-236.
42. NOEL, J. P., H. E. HAMM and P. B. SIGLER, 1993 The 2.2 A crystal structure of transducin-alpha complexed with GTP gamma S. Nature 366: 654-663.
43. NURRISH, S., L. SEGALAT and J. M. KAPLAN, 1999 Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231-242.
44. PANCRAZIO, J. J., W. K. PARK and C. LYNCH, III, 1993 Inhalational anesthetic actions on voltage-gated ion currents of bovine adrenal chromaffin cells. Mol. Pharmacol. 43: 783-794.
45. PATEL, A. J., E. HONORE, F. LESAGE, M. FINK, G. ROMEY et al., 1999 Inhalational anesthetics activate two-pore-domain background K+ channels. Nat. Neurosci. 2: 422-426.
46. PEROUANSKY, M., D. BARANOV, M. SALMAN and Y. YAARI, 1995 Effects of halothane on glutamate receptor-mediated excitatory postsynaptic currents. Anesthesiology 83: 109-119.
47. PHELAN, P., and T. A. STARICH, 2001 Innexins get into the gap. BioEssays 23: 388-396.
48. PHELAN, P., J. P. BACON, J. A. DAVIES, L. A. STEBBINGS, M. G. TODMAN et al., 1998 Innexins: a family of invertebrate gap-junction proteins. Trends Genet. 14: 348-349.
49. POCOCK, G., and C. D. RICHARDS, 1991 Cellular mechanisms in general anaesthesia. Br. J. Anaesth. 66: 116-128.
50. POIRIER, M. A., W. XIAO, J. C. MACOSKO, C. CHAN, Y. K. SHIN et al., 1998 The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5: 765-769.
51. RAJARAM, S., M. M. SEDENSKY and P. G. MORGAN, 1998 Unc-1: a stomatin homologue controls sensitivity to volatile anesthetics in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95: 8761-8766.
52. RAJARAM, S., T. L. SPANGLER, M. M. SEDENSKY and P. G. MORGAN, 1999 A stomatin and a degenerin interact to control anesthetic sensitivity in Caenorhabditis elegans. Genetics 153: 1673-1682.
53. RAND, J. B., and M. L. NONET, 1997 Synaptic transmission, pp. 611-643 in C. elegans II, edited by D. L. RIDDLE, T. BLUMENTHAL, B. J. MEYER and J. R. PRIESS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. REINER, D. J., E. M. NEWTON, H. TIAN and J. H. THOMAS, 1999 Diverse behavioural defects caused by mutations in Caenorhabditis elegans unc-43 CaM kinase II. Nature 402: 199-203.
55. RIZO, J., and T. C. SUDHOF, 2002 Snares and Munc18 in synaptic vesicle fusion. Nat. Rev. Neurosci. 3: 641-653.
56. q signaling network. Genetics 156: 1069-1082.
57. ROBATZEK, M., T. NIACARIS, K. STEGER, L. AVERY and J. H. THOMAS, 2001 eat-11 encodes GPB-2, a Gbeta(5) ortholog that interacts with G(o)alpha and G(q)alpha to regulate C. elegans behavior. Curr. Biol. 11: 288-293.
58. RONGO, C., and J. M. KAPLAN, 1999 CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402: 195-199.
59. SAIFEE, O., L. WEI and M. L. NONET, 1998 The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol. Biol. Cell 9: 1235-1252.
60. SCHLAME, M., and H. C. HEMMINGS, JR., 1995 Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by a presynaptic mechanism. Anesthesiology 82: 1406-1416.
61. SEDENSKY, M. M., and P. M. MENEELY, 1987 Genetic analysis of halothane sensitivity in Caenorhabditis elegans. Science 236:952-954.
62. STARICH, T. A., R. Y. LEE, C. PANZARELLA, L. AVERY and J. E. SHAW, 1996 eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling. J. Cell Biol. 134: 537-548.
63. STRINGHAM, E. G., D. K. DIXON, D. JONES and E. P. CANDIDO, 1992 Temporal and spatial expression patterns of the small heat shock (hspl6) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3: 221-233.
64. SUTTON, R. B., D. FASSHAUER, R. JAHN and A. T. BRUNGER, 1998 Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353.
65. TAKENOSHITA, M., and T. TAKAHASHI, 1987 Mechanisms of halothane action on synaptic transmission in motoneurons of the newborn rat spinal cord in vitro. Brain Res. 402: 303-310.
66. TAVERNARAKIS, N., W. SHREFFLER, S. WANG and M. DRISCOLL, 1997 unc-8, a Deg/EnaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 18: 107-119.
67. TINKLENBERG, J. A., I. S. SEGAL, T. Z. Guo and M. MAZE, 1991 Analysis of anesthetic action on the potassium channels of the Shaker mutant of Drosophila. Ann. NY Acad. Sci. 625: 532-539.
68. qα signaling network through interactions with the regulator of G-protein signaling proteins EGL-10 and EAT-16. Genetics 158: 221-235.
69. VAN SWINDEREN, B., O. SAIFEE, L. SHEBESTER, R. ROBERSON, M. L. NONET et al., 1999 A neomorphic syntaxin mutation blocks volatile-anesthetic action in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 96: 2479-2484.
70. VAN SWINDEREN, B., L. B. METZ, L. D. SHEBESTER, J. E. MENDEL, P. W. STERNBERG et al., 2001 Goalpha regulates volatile anesthetic action in Caenorhabditis elegans. Genetics 158: 643-655.
71. VAN SWINDEREN, B., L. B. METZ, L. D. SHEBESTER and C. M. CROWDER, 2002 A Caenorhabditis elegans pheromone antagonizes volatile anesthetic action through a Go-coupled pathway. Genetics 161: 109-119.
72. WANG, Z. W., O. SAIFEE, M. L. NONET and L. SALKOFF, 2001 SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32: 867-881.
73. WAUD, D. R., 1972 On biological assays involving quantal responses. J. Pharmacol. Exp. Ther. 183: 577-607.
74. XIAO, W., M. A. POIRIER, M. K. BENNETT and Y. K. SHIN, 2001 The neuronal t-SNARE complex is a parallel four-helix bundle. Nat. Struct. Biol. 8: 308-311.
75. YAMAKURA, T., E. BERTACCINI, J. R. TRUDELL and R. A. HARRIS, 2001 Anesthetics and ion channels: molecular models and sites of action. Annu. Rev. Pharmacol. Toxicol. 41: 23-51.
76. ZORYCHTA, E., and R. CAPEK, 1978 Depression of spinal monosynaptic transmission by diethyl ether: quantal analysis of unitary synaptic potentials. J. Pharmacol. Exp. Ther. 207: 825-836.