Isoflurane inhibits synaptic vesicle exocytosis through reduced Ca2+ influx, not Ca2+-exocytosis coupling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 38, 2015, Pages 11959-11964

  Baumgart, Joel P ^a   Zhou, Zhen Yu ^a   Hara, Masato ^a,b   Cook, Daniel C ^a   Hoppa, Michael B ^a,c   Ryan, Timothy A ^a   Hemmings, Hugh C ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Lamont Doherty Earth Observatory   (United States)

Author keywords

GCaMP3; Live cell imaging; Mechanisms of anesthesia; Phlourin; Presynaptic

Indexed keywords

CALCIUM ION; ISOFLURANE; 4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM; GLUTAMIC ACID DERIVATIVE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CALCIUM TRANSPORT; CONFERENCE PAPER; CONTROLLED STUDY; EC50; ENDOCYTOSIS; EXOCYTOSIS; NERVE ENDING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; DRUG EFFECTS; KINETICS; METABOLISM; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; CALCIUM; EXOCYTOSIS; GABAERGIC NEURONS; GLUTAMATES; ISOFLURANE; KINETICS; PRESYNAPTIC TERMINALS; RATS, SPRAGUE-DAWLEY; SYNAPTIC VESICLES;

EID: 84942863247     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500525112     Document Type: Article

References (69)

1. Hemmings HC, Jr, et al. (2005) Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol Sci 26(10):503-510.
2. Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322(5903):876-880.
3. Lewis LD, et al. (2012) Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proc Natl Acad Sci USA 109(49):E3377-E3386.
4. Blain-Moraes S, et al. (2015) Neurophysiological correlates of sevoflurane-induced unconsciousness. Anesthesiology 122(2):307-316.
5. Schlame M, Hemmings HC, Jr (1995) Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by a presynaptic mechanism. Anesthesiology 82(6):1406-1416.
6. 2+ transients and glutamate release in isolated cerebral synaptosomes. Anesthesiology 83(3):593-603.
7. Hemmings HC, Jr, Yan W, Westphalen RI, Ryan TA (2005) The general anesthetic isoflurane depresses synaptic vesicle exocytosis. Mol Pharmacol 67(5):1591-1599.
8. Herring BE, Xie Z, Marks J, Fox AP (2009) Isoflurane inhibits the neurotransmitter release machinery. J Neurophysiol 102(2):1265-1273.
9. Xie Z, et al. (2013) Interaction of anesthetics with neurotransmitter release machinery proteins. J Neurophysiol 109(3):758-767.
10. Augustine GJ (2001) How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11(3):320-326.
11. Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77:615-641.
12. Westphalen RI, Hemmings HC, Jr (2006) Volatile anesthetic effects on glutamate versus GABA release from isolated rat cortical nerve terminals: 4-aminopyridineevoked release. J Pharmacol Exp Ther 316(1):216-223.
13. Franks NP (2008) General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9(5):370-386.
14. Brown EN, Purdon PL, Van Dort CJ (2011) General anesthesia and altered states of arousal: A systems neuroscience analysis. Annu Rev Neurosci 34:601-628.
15. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79(4):2199-2208.
16. Sankaranarayanan S, Ryan TA (2001) Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4(2):129-136.
17. Taheri S, et al. (1991) What solvent best represents the site of action of inhaled anesthetics in humans, rats, and dogs? Anesth Analg 72(5):627-634.
18. Kim SH, Ryan TA (2010) CDK5 serves as a major control point in neurotransmitter release. Neuron 67(5):797-809.
19. Hoppa MB, Lana B, Margas W, Dolphin AC, Ryan TA (2012) α2δ expression sets presynaptic calcium channel abundance and release probability. Nature 486(7401):122-125.
20. Tian L, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875-881.
21. Ariel P, Ryan TA (2010) Optical mapping of release properties in synapses. Front Neural Circuits 4:1-10.
22. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23(2):399-409.
23. Dobie FA, Craig AM (2011) Inhibitory synapse dynamics: Coordinated presynaptic and postsynaptic mobility and the major contribution of recycled vesicles to new synapse formation. J Neurosci 31(29):10481-10493.
24. Dittman J, Ryan TA (2009) Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25:133-160.
25. Meir A, et al. (1999) Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev 79(3):1019-1088.
26. Westphalen RI, Desai KM, Hemmings HC, Jr (2013) Presynaptic inhibition of the release of multiple major central nervous system neurotransmitter types by the inhaled anaesthetic isoflurane. Br J Anaesth 110(4):592-599.
27. Bragina L, et al. (2011) Analysis of synaptotagmin, SV2, and rab3 expression in cortical glutamatergic and GABAergic axon terminals. Front Cell Neurosci 5:32.
28. 2+ channels: A functional patchwork. Trends Neurosci 26(12):683-687.
29. Grønborg M, et al. (2010) Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J Neurosci 30(1):2-12.
30. Moulder KL, et al. (2007) Vesicle pool heterogeneity at hippocampal glutamate and GABA synapses. J Neurosci 27(37):9846-9854.
31. Xu J, Mashimo T, Südhof TC (2007) Synaptotagmin-1, -2, and -9: Ca (2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54(4):567-581.
32. Rahamimoff R, et al. (1999) Multitude of ion channels in the regulation of transmitter release. Philos Trans R Soc Lond B Biol Sci 354(1381):281-288.
33. Vacher H, Mohapatra DP, Trimmer JS (2008) Localization and targeting of voltagedependent ion channels in mammalian central neurons. Physiol Rev 88(4):1407-1447.
34. Martire M, et al. (2010) Pre-synaptic BK channels selectively control glutamate versus GABA release from cortical and hippocampal nerve terminals. J Neurochem 115(2):411-422.
35. Debanne D, Bialowas A, Rama S (2013) What are the mechanisms for analogue and digital signalling in the brain? Nat Rev Neurosci 14(1):63-69.
36. 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.
37. Bieda MC, MacIver MB (2004) Major role for tonic GABAA conductances in anesthetic suppression of intrinsic neuronal excitability. J Neurophysiol 92(3):1658-1667.
38. Oose Y, et al. (2012) Imbalanced suppression of excitatory and inhibitory synaptic transmission onto mouse striatal projection neurons during induction of anesthesia with sevoflurane in vitro. Eur J Neurosci 35(9):1396-1405.
39. Mashour GA (2014) Top-down mechanisms of anesthetic-induced unconsciousness. Front Syst Neurosci 8:115.
40. Sonner JM, et al. (2003) Inhaled anesthetics and immobility: Mechanisms, mysteries, and minimum alveolar anesthetic concentration. Anesth Analg 97(3):718-740.
41. Jurd R, et al. (2003) General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA (A) receptor beta3 subunit. FASEB J 17(2):250-252.
42. Zhang Y, et al. (2004) Gamma-aminobutyric acidA receptors do not mediate the immobility produced by isoflurane. Anesth Analg 99(1):85-90.
43. Liao M, et al. (2005) Beta3-containing gamma-aminobutyric acidA receptors are not major targets for the amnesic and immobilizing actions of isoflurane. Anesth Analg 101(2):412-418.
44. Herold KF, Hemmings HC, Jr (2012) Sodium channels as targets for volatile anesthetics. Front Pharmacol 3:50.
45. Franks NP, Honoré E (2004) The TREK K2P channels and their role in general anaesthesia and neuroprotection. Trends Pharmacol Sci 25(11):601-608.
46. Study RE (1994) Isoflurane inhibits multiple voltage-gated calcium currents in hippocampal pyramidal neurons. Anesthesiology 81(1):104-116.
47. Westphalen RI, Hemmings HC, Jr (2003) Effects of isoflurane and propofol on glutamate and GABA transporters in isolated cortical nerve terminals. Anesthesiology 98(2):364-372.
48. Cechova S, Zuo Z (2006) Inhibition of glutamate transporters increases the minimum alveolar concentration for isoflurane in rats. Br J Anaesth 97(2):192-195.
49. Nagele P, et al. (2005) Volatile anesthetics bind rat synaptic snare proteins. Anesthesiology 103(4):768-778.
50. Wu XS, Sun JY, Evers AS, Crowder M, Wu LG (2004) Isoflurane inhibits transmitter release and the presynaptic action potential. Anesthesiology 100(3):663-670.
51. Ouyang W, Hemmings HC, Jr (2005) Depression by isoflurane of the action potential and underlying voltage-gated ion currents in isolated rat neurohypophysial nerve terminals. J Pharmacol Exp Ther 312(2):801-808.
52. Joksovic PM, et al. (2009) Isoflurane-sensitive presynaptic R-type calcium channels contribute to inhibitory synaptic transmission in the rat thalamus. J Neurosci 29(5):1434-1445.
53. Rama S, Zbili M, Debanne D (2014) Modulation of spike-evoked synaptic transmission: The role of presynaptic calcium and potassium channels. Biochim Biophys Acta 1853(9):1933-1939.
54. Hochbaum DR, et al. (2014) All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat Methods 11(8):825-833.
55. Hoppa MB, Gouzer G, Armbruster M, Ryan TA (2014) Control and plasticity of the presynaptic action potential waveform at small CNS nerve terminals. Neuron 84(4):778-789.
56. Verhage M, et al. (1991) Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6(4):517-524.
57. Elliott EM, Malouf AT, Catterall WA (1995) Role of calcium channel subtypes in calcium transients in hippocampal CA3 neurons. J Neurosci 15(10):6433-6444.
58. Balaji J, Ryan TA (2007) Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc Natl Acad Sci USA 104(51):20576-20581.
59. Solt K, Forman SA (2007) Correlating the clinical actions and molecular mechanisms of general anesthetics. Curr Opin Anaesthesiol 20(4):300-306.
60. Akeju O, et al. (2014) Effects of sevoflurane and propofol on frontal electroencephalogram power and coherence. Anesthesiology 121(5):990-998.
61. MacIver MB (2014) Anesthetic agent-specific effects on synaptic inhibition. Anesth Analg 119(3):558-569.
62. Zhang Y, et al. (2010) Bidirectional modulation of isoflurane potency by intrathecal tetrodotoxin and veratridine in rats. Br J Pharmacol 159(4):872-878.
63. Jinks SL, Bravo M, Hayes SG (2008) Volatile anesthetic effects on midbrain-elicited locomotion suggest that the locomotor network in the ventral spinal cord is the primary site for immobility. Anesthesiology 108(6):1016-1024.
64. Lukatch HS, Kiddoo CE, Maciver MB (2005) Anesthetic-induced burst suppression EEG activity requires glutamate-mediated excitatory synaptic transmission. Cereb Cortex 15(9):1322-1331.
65. Kenny JD, Westover MB, Ching S, Brown EN, Solt K (2014) Propofol and sevoflurane induce distinct burst suppression patterns in rats. Front Syst Neurosci 8:237.
66. Ratnakumari L, Hemmings HC, Jr (1998) Inhibition of presynaptic sodium channels by halothane. Anesthesiology 88(4):1043-1054.
67. Ryan TA (1999) Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 19(4):1317-1323.
68. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394(6689):192-195.
69. Kim SH, Ryan TA (2009) A distributed set of interactions controls mu2 functionality in the role of AP-2 as a sorting adaptor in synaptic vesicle endocytosis. J Biol Chem 284(47):32803-32812.