Sodium channels and the synaptic mechanisms of inhaled anaesthetics

British Journal of Anaesthesia

Volumn 103, Issue 1, 2009, Pages 61-69

  Hemmings Jr , H C ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Anaesthetics volatile; Anaesthetics volatile, halogenated hydrocarbons; Nerve, neurotransmitters; Pharmacology, anaesthetic action; Pharmacology, neurotransmission

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; INHALATION ANESTHETIC AGENT; ISOFLURANE; PROPOFOL; RILUZOLE; VOLTAGE GATED SODIUM CHANNEL; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; SODIUM CHANNEL;

ACTION POTENTIAL; CELL ISOLATION; DRUG EFFECT; DRUG MECHANISM; EXCITATORY POSTSYNAPTIC POTENTIAL; GENERAL ANESTHESIA; NERVE CELL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SYNAPTIC TRANSMISSION; CHANNEL GATING; HUMAN; METABOLISM; PHYSIOLOGY; SYNAPSE;

ANESTHETICS, INHALATION; HUMANS; ION CHANNEL GATING; NEUROTRANSMITTER AGENTS; SODIUM CHANNELS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 67650716519     PISSN: 00070912     EISSN: 14716771     Source Type: Journal    
DOI: 10.1093/bja/aep144     Document Type: Review

References (108)

1. Antognini JF, Schwartz K. Exaggerated anesthetic requirements in the preferentially anesthetized brain. Anesthesiology 1993; 79: 1244-9
2. Banks MI, Pearce RA. Dual actions of volatile anesthetics on GABA(A) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology 1999; 90: 120-34
3. Bean BP, Shrager P, Goldstein DA. Modification of sodium and potassium channel gating kinetics by ether and halothane. J Gen Physiol 1981; 77: 233-53
4. Berg-Johnsen J, Langmoen IA. The effect of isoflurane on unmyelinated and myelinated fibres in the rat brain. Acta Physiology Scand 1986; 127: 87-93
5. Berg-Johnsen J, Langmoen IA. The effects of isoflurane on excitatory synaptic transmission in the rat hippocampus. Acta Anaesthesiol Scand 1992; 36: 350-4
6. A conductances in anesthetic suppression of intrinsic neuronal excitability. J Neurophysiol 2004; 92: 1658-67
7. Brockmeyer DM, Kendig JJ. Selective effects of ketamine on amino acid-mediated pathways in neonatal rat spinal cord. Br J Anaesth 1995; 74: 79-84
8. A receptor-mediated inhibition. Anesthesiology 2000; 92: 1067-73
9. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000; 26: 13-25
10. Cestele S, Catterall WA. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 2000; 82: 883-92
11. de Sousa SL, Dickinson R, Lieb WR, Franks NP. Contrasting synaptic actions of the inhalational general anesthetics isoflurane and xenon. Anesthesiology 2000; 92: 1055-66
12. Dickinson R, Peterson BK, Banks P, et al. Competitive inhibition at the glycine site of the N-methyl-D-aspartate receptor by the anesthetics xenon and isoflurane: evidence from molecular modeling and electrophysiology. Anesthesiology 2007; 107: 756-67
13. Dildy-Mayfield JE, Eger E, III, Harris RA. Anesthetics produce subunit-selective actions on glutamate receptors. J Pharmacol Exp Ther 1996; 276: 1058-65
14. Dodge FAJ, Rahamimoff R. On the relationship between calcium concentration and the amplitude of the end-plate potential. J Physiol 1967; 189: 90P-92P
15. Eger EI II, Raines DE, Shafer SL, Hemmings HC, Jr, Sonner JM. Is a new paradigm needed to explain how inhaled anesthetics produce immobility? Anesth Analg 2008; 107: 832-48
16. Eilers H, Kindler CH, Bickler PE. Different effects of volatile anesthetics and polyhalogenated alkanes on depolarization-evoked glutamate release in rat cortical brain slices. Anesth Analg 1999; 88: 1168-74
17. Flood P, Ramirez-Latorre J, Role L. Alpha 4 beta 2 neuronal nicotinic acetylcholine receptors in the central nervous system are inhibited by isoflurane and propofol, but alpha 7-type nicotinic acetylcholine receptors are unaffected. Anesthesiology 1997; 86: 859-65
18. Franks NP, Honoré E. The TREK K2P channels and their role in general anaesthesia and neuroprotection. Trends Pharmacol Sci 2004; 25: 601-8
19. Franks NP, Lieb WR. Molecular and cellular mechanisms of general anaesthesia . Nature 1994; 367: 607-13
20. 2+ sensor. Br J Anaesth 2005; 95: 216-21
21. Gage PW, Robertson B. Prolongation of inhibitory postsynaptic currents by pentobarbitone, halothane and ketamine in CA1 pyramidal cells in rat hippocampus. Br J Pharmacol 1985; 85: 675-81
22. + channel KCNK5. Anesthesiology 2000; 92: 1722-30
23. + channels are a novel target for the anesthetic gases xenon, nitrous oxide, and cyclopropane. Mol Pharmacol 2004; 65: 443-52
24. Hall AC, Lieb WR, Franks NP. Insensitivity of P-type calcium channels to inhalational and intravenous general anesthetics. Anesthesiology 1994; 81: 117-23
25. Haseneder R, Kratzer S, Kochs E, et al. Xenon reduces N-methyl-D-aspartate and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor-mediated synaptic transmission in the amygdala. Anesthesiology 2008; 109: 998-1006
26. Haydon DA, Urban BW. The effects of some inhalation anaesthetics on the sodium current of the squid giant axon. J Physiol 1983; 341: 429-39
27. Hemmings HC, Jr, Akabas MH, Goldstein PA, Trudell JR, Orser BA, Harrison NL. Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol Sci 2005; 26: 503-10
28. Hemmings HC, Jr, Yan W, Westphalen RI, Ryan TA. The general anesthetic isoflurane depresses synaptic vesicle exocytosis. Mol Pharmacol 2005; 67: 1591-9
29. Herold KF, Nau C, Ouyang W, Hemmings HC, Jr. Isoflurane inhibits the tetrodotoxin-resistant voltage-gated sodium channel Nav1.8. Anesthesiology 2009; in press
30. Jones MV, Harrison NL. Effects of volatile anesthetics on the kinetics of inhibitory postsynaptic currents in cultured rat hippocampal neurons. J Neurophysiol 1993; 70: 1339-49
31. Jurd R, Arras M, Lambert S, et al. General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit. FASEB J 2003; 17: 250-2
32. Kamatchi GL, Chan CK, Snutch T, Durieux ME, Lynch C, III. Volatile anesthetic inhibition of neuronal Ca channel currents expressed in Xenopus oocytes. Brain Res 1999; 831: 85-96
33. Kullman DM, Martin RL, Redman SJ. Reduction by general anesthetics of group Ia excitatory postsynaptic potentials and currents in the cat spinal cord. J Physiol (London) 1989; 412: 277-96
34. Larrabee MG, Posternak JM. Selective action of anesthetics on synapses and axons in mammalian sympathetic ganglia. J Neurophysiol 1952; 15: 91-114
35. 2+-dependent glutamate release from rat cerebral cortex. Brain Res 1994; 663: 335-7
36. Liachenko S, Tang P, Somogyi GT, Xu Y. Concentration-dependent isoflurane effects on depolarization-evoked gluta-mate and GABA outflows from mouse brain slices. Br J Pharmacol 1999; 127: 131-8
37. Liao M, Sonner JM, Jurd R, et al. Beta3-containing gamma-aminobutyric acidA receptors are not major targets for the amnesic and immobilizing actions of isoflurane. Anesth Analg 2005; 101: 412-8
38. Lingamaneni R, Birch ML, Hemmings HC, Jr. Widespread inhibition of sodium channel-dependent glutamate release from isolated nerve terminals by isoflurane and propofol. Anesthesiology 2001; 95: 1460-6
39. MacDermott AB, Role LW, Siegelbaum SA. Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 1999; 22: 443-85
40. MacIver MB, Mikulec AA, Amagasu SM, Monroe FA. Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 1996; 85: 823-34
41. Meir A, Ginsburg S, Butkevich A, et al. Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev 1999; 79: 1019-88
42. Mennerick S, Jevtovic-Todorovic V, Todorovic SM, Shen W, Olney JW, Zorumski CF. Effect of nitrous oxide on excitatory and inhibitory synaptic transmission in hippocampal cultures. J Neurosci 1998; 18: 9716-26
43. 2+ transients and glutamate release in isolated cerebral synaptosomes. Anesthesiology 1995; 83: 593-603
44. Mikulec AA, Pittson S, Amagasu SM, Monroe FA, Maclver MB. Halothane depresses action potential conduction in hippocam-pal axons. Brain Res 1998; 796: 231-8
45. Minami K, Wick MJ, Stern-Bach Y, et al. Sites of volatile anesthetic action on kainate (glutamate receptor 6) receptors. J Biol Chem 1998; 273: 8248-55
46. 3H]GABA release from rat cortical synaptosomes. Anesthesiology 1998; 89: 919-28
47. Nagele P, Mendel JB, Placzek WJ, Scott BA, d'Avignon DA, Crowder CM. Volatile anesthetics bind rat synaptic SNARE proteins. Anesthesiology 2005; 103: 768-78
48. Nicholls DG. The glutamatergic nerve terminal. Eur J Biochem 1993; 212: 613-31
49. Nicoll RA, Eccles JC, Oshima T, Rubia F. Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature 1975; 258: 625-6
50. Nikonorov IM, Blanck TJ, Recio-Pinto E. The effects of halothane on single human neuronal L-type calcium channels. Anesth Analg 1998; 86: 885-95
51. Nishikawa K-I, Kidokoro Y. Halothane presynaptically depresses synaptic transmission in wild-type Drosophila larvae but not halothane-resistant (har) mutants. Anesthesiology 1999; 90: 1691-7
52. Nishikawa K-I, MacIver MB. Excitatory synaptic transmission mediated by NMDA receptors is more sensitive to isoflurane than are non-NMDA receptor-mediated responses. Anesthesiology 2000; 92: 228-36
53. Ouanonou A, Zhang Y, Zhang L. Changes in the calcium dependence of glutamate transmission in the hippocampal CA1 region after brief hypoxia-hypoglycemia. J Neurophysiol 1999; 82: 1147-55
54. OuYang W, Hemmings HC, Jr. Depression by isoflurane of the action potential and underlying voltage-gated ion currents in isolated rat neurohypophysial nerve terminals. J Pharmacol Exp Ther 2005; 312: 801-8
55. + channels. Anesthesiology 2007; 107: 91-8
56. Ouyang W, Herold KF, Hemmings HC, Jr. Comparative effects of halogenated inhaled anesthetics on voltage-gated Na+ channel function. Anesthesiology 2009; 110: 582-90
57. OuYang W, Jih T-y, Zhang T-t, Correa AM, Hemmings HC, Jr. Isoflurane inhibits NaChBac, a prokaryotic voltage-gated sodium channel. J Pharmacol Exp Ther 2007; 322: 1076-83
58. + channels in isolated rat neurohypophy-sial nerve terminals. Mol Pharmacol 2003; 64: 373-81
59. + channels. Anesthesiology 2001; 95: 1013-21
60. + channels. Nature Neurosci 1999; 2: 422-6
61. Perouansky M, Baranov D, Salamn M, Yaari Y. Effects of halothane on glutamate receptor-mediated excitatory postsynaptic currents: A patch-clamp study in adult mouse hippocampal slices. Anesthesiology 1995; 83: 109-19
62. Perouansky M, Hemmings HC Jr. Presynaptic actions of general anesthetics. In: Antognini JF, Carlens E, Raines D, eds. Neural Mechanisms of Anesthesia. Totowa, NJ: Humana Press, 2003; 345-70
63. Perouansky M, Hemmings HC, Jr, Pearce RA. Anesthetic effects on glutamatergic transmission: Lessons learned from a large synapse. Anesthesiology 2004; 100: 470-2
64. Pittson S, Himmel AM, MacIver MB. Multiple synaptic and membrane sites of anesthetic action in the CA1 region of rat hippocampal slices. BMC Neurosci 2004; 5: 52
65. + channels. Proc Natl Acad Sci USA 1996; 93: 9270-5
66. Rampil IJ, Mason P, Singh H. Anesthetic potency (MAC) is independent of forebrain structures in the rat. Anesthesiology 1993; 78: 707-12
67. Ratnakumari L, Hemmings HC, Jr. Inhibition by propofol of [3H]batrachotoxinin-A 20-α-benzoate binding to voltage-dependent sodium channels in rat cortical synaptosomes. Br J Pharmacol 1996; 119: 1498-504
68. Ratnakumari L, Hemmings HC, Jr. Effects of propofol on sodium channel-dependent sodium influx and glutamate release in rat cerebrocortical synaptosomes. Anesthesiology 1997; 86: 428-39
69. Ratnakumari L, Hemmings HC, Jr. Inhibition by presynaptic sodium channels by halothane. Anesthesiology 1998; 88: 1043-54
70. Ratnakumari L, Vysotskaya TN, Duch DS, Hemmings HC Jr. Differential effects of anesthetic and nonanesthetic cyclobutanes on neuronal voltage-gated sodium channels. Anesthesiology 2000; 92: 529-41
71. Rehberg B, Xiao Y-H, Duch DS. Central nervous system sodium channels are significantly suppressed at clinical concentrations of volatile anesthetics. Anesthesiology 1996; 84: 1223-33
72. 2+ channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures. J Neurosci 1997; 17: 2738-45
73. Richards CD, Smaje JC. Anaesthetics depress the sensitivity of cortical neurones to L-glutamate. Br J Pharmacol 1976; 58: 347-57
74. Richards CD, White AE. The actions of volatile anaesthetics on synaptic transmission in the dentate gyrus. J Physiol 1975; 252: 241-57
75. Rudolph U, Antkowiak B. Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 2004; 5: 709-20
76. Sandstrom DJ. Isoflurane depresses glutamate release by reducing neuronal excitability at the Drosophila neuromuscular junction. J Physiol 2004; 558: 489-502
77. Schlame M, Hemmings HC, Jr. Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by a pre-synaptic mechanism. Anesthesiology 1995; 82: 1406-16
78. + channels. J Pharmacol Exp Ther 2004; 309: 987-94
79. + current and I(h) by an inhalational anaesthetic and neurotransmitters in rat brainstem motoneurones. J Physiol 2002; 541: 717-29
80. Solt K, Eger EI, II, Raines DE. Differential modulation of human N-methyl-D-aspartate receptors by structurally diverse general anesthetics. Anesth Analg 2006; 102: 1407-11
81. Sonner JM, Antognini JF, Dutton RC, et al. Inhaled anesthetics and immobility: mechanisms, mysteries, and minimum alveolar anesthetic concentration. Anesth Analg 2003; 97: 718-40
82. Stadnicka A, Kwok WM, Hartmann HA, Bosnjak ZJ. Effects of halothane and isoflurane on fast and slow inactivation of human heart hH1a sodium channels. Anesthesiology 1999; 90: 1671-83
83. Stowe DF, Rehmert GC, Kwok WM, et al. Xenon does not alter cardiac function or major cation currents in isolated guinea pig hearts or myocytes. Anesthesiology 2000; 92: 516-22
84. 2+ currents in hippocampal pyramidal neurons. Anesthesiology 1994; 81: 104-16
85. Stuth EA, Krolo M, Tonkovic-Capin M, Hopp FA, Kampine JP, Zuperku EJ. Effects of halothane on synaptic neurotransmission to medullary expiratory neurons in the ventral respiratory group of dogs. Anesthesiology 1999; 91: 804-14
86. Südhof TC. The synaptic vesicle cycle. Ann Rev Neurosci 2004; 27: 509-47
87. Tanifuji Y, Eger EI, II. Brain sodium, potassium, and osmolality: Effects on anesthetic requirement. Anesth Analg 1978; 57: 404-10
88. van Swinderen B, Saifee O, Shebester L, Roberson R, Nonet ML, Crowder CM. A neomorphic syntaxin mutation blocks volatile-anesthetic action in Caenorhabditis elegans. Proc Natl Acad Sci USA 1999; 96: 2479-84
89. Violet JM, Downie DL, Nakisa RC, Lieb WR, Franks NP. Differential sensitivities of mammalian neuronal and muscle nic-otinic acetylcholine receptors to general anesthetics. Anesthesiology 1997; 86: 866-74
90. Wakamori M, Ikemoto Y, Akaike N. Effects of two volatile anesthetics and a volatile convulsant on the excitatory and inhibitory amino acid responses in dissociated CNS neurons of the rat. J Neurophysiol 1991; 66: 2014-21
91. Wakasugi M, Hirota K, Roth S, Ito Y. The effects of general anesthetics agents on excitatory and inhibitor synaptic transmission in area CA1 of the rat hippocampus in vitro. Anesth Analg 1999; 88: 676-80
92. 2+ current in neurohypophysial terminals preferentially regulates oxytocin secretion. J Neurosci 1999; 19: 9235-41
93. Weakly JN. Effect of barbiturate on quantal synaptic transmission in spinal motoneurones. J Physiol (London) 1969; 204: 63-77
94. Westphalen RI, Hemmings HC, Jr. Effects of isoflurane and pro-pofol on glutamate and GABA transporters in isolated cortical nerve terminals. Anesthesiology 2003; 98: 364-72
95. Westphalen RI, Hemmings HC, Jr. Selective depression by general anesthetics of glutamate vs GABA release from isolated nerve terminals. J Pharmacol Exp Ther 2003; 304: 1188-96
96. Westphalen RI, Hemmings HC, Jr. Volatile anesthetic effects on glutamate versus GABA release from isolated rat cortical nerve terminals: Basal release. J Pharmacol Exp Ther 2006; 316: 208-15
97. Westphalen RI, Hemmings HC, Jr. Volatile anesthetic effects on glutamate versus GABA release from isolated rat cortical nerve terminals: 4-Aminopyridine evoked release. J Pharmacol Exp Ther 2006; 316: 216-23
98. Wu LG, Saggau P. Presynaptic inhibition of elicited neurotrans-mitter release. Trends Neurosci 1997; 20: 204-12
99. Wu LG, Westenbroek RE, Borst JGG, Catterall WA, Sakmann B. Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J Neurosci 1999; 19: 726-36
100. Wu XS, Sun JY, Evers AS, Crowder M, Wu LG. Isoflurane inhibits transmitter release and the presynaptic action potential. Anesthesiology 2004; 100: 663-70
101. Xing Y, Zhang Y, Stabernack CR, Eger EI II, Gray AT. The use of the potassium channel activator riluzole to test whether potassium channels mediate the capacity of isoflurane to produce immobility. Anesth Analg 2003; 97: 1020-4
102. Yamakura T, Bertaccini E, Trudell JR, Harris RA. Anesthetics and ion channels: molecular models and sites of action. Annu Rev Pharmacol Toxicol 2001; 41: 23-51
103. Yamakura T, Harris RA. Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels. Comparison with isoflurane and ethanol. Anesthesiology 2000; 93: 1095-101
104. Yang J, Zorumski CF. Effects of isoflurane on N-methyl-D-aspartate gated ion channels in cultured rat hippocampal neurons. Ann NY Acad Sci 1991; 625: 287-9
105. Zhang Y, Laster MJ, Eger EI II, Sharma M, Sonner JM. Lidocaine, MK-801, and MAC. Anesth Analg 2007; 104: 1098-102
106. Zhang Y, Sharma M, Eger EI, II, Laster MJ, Hemmings HC, Jr, Harris RA. Intrathecal veratridine administration increases MAC in rats. Anesth Analg 2008; 107: 875-8
107. Zhang Y, Sonner JM, Eger EI II, et al. Gamma-aminobutyric acidA receptors do not mediate the immobility produced by isoflurane. Anesth Analg 2004; 99: 85-90
108. Zimmerman SA, Jones MV, Harrison NL. Potentiation of gamma-aminobutyric acid A receptor Cl-current correlates with in vivo anesthetic potency. J Pharmacol Exp Ther 1994; 270: 987-91