Dual effects of neuroprotection and neurotoxicity by general anesthetics: Role of intracellular calcium homeostasis

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 47, Issue , 2013, Pages 156-161

  Wei, Huafeng ^a   Inan, Saadet ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Anesthesia; Anesthetics; Calcium; Neurodegeneration; Neuroprotection; Neurotoxicity

Indexed keywords

ANESTHETIC AGENT; DANTROLENE; DESFLURANE; DIAZOXIDE; HALOTHANE; INHALATION ANESTHETIC AGENT; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ISOFLURANE; KETAMINE; MIDAZOLAM; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B ANTAGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PROPOFOL; RYANODINE RECEPTOR; SEVOFLURANE; UNCLASSIFIED DRUG; XENON; XESTOSPONGIN C;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; DRUG EFFECT; DRUG MECHANISM; ENDOPLASMIC RETICULUM; HUMAN; INTRACELLULAR MEMBRANE; NERVE CELL LESION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN;

3-(4,5-DIMETHYLTHIAZOL-2-YL)-2,5-DIPHENYLTETRAZOLIUM BROMIDE; 5-HD; 5-HYDROXYDECANOATE; AKT; ANESTHESIA; ANESTHETICS; CALCIUM; ENDOPLASMIC RETICULUM; ER; ERK; EXTRACELLULAR SIGNAL-REGULATED KINASES; GABA; GAMMA-AMINOBUTYRIC ACID; GLYCOGEN SYNTHASE KINASE 3Β; GSK3Β; INSP(3) RECEPTORS; INSP(3)R; LACTATE DEHYDROGENASE; LDH; LONG TERM POTENTIATION; LTP; MAPK; MITOCHONDRIAL PERMEABILITY TRANSITION PORES; MITOGEN-ACTIVATED PROTEIN KINASE; MPTP; MTT; N-METHYL-D-ASPARTATE; NEURODEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NMDA; OGD; OXYGEN-GLUCOSE DEPRIVATION; PROTEIN KINASE B; RYANODINE RECEPTORS; RYRS; VDCC; VOLTAGE DEPENDENT CA(2+) CHANNELS; XC; XESTOSPONGIN C;

ANESTHETICS, GENERAL; ANIMALS; CALCIUM; HOMEOSTASIS; HUMANS; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES;

EID: 84887171489     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.05.009     Document Type: Article

References (76)

1. Adamczyk S., Robin E., Simerabet M., Kipnis E., Tavernier B., Vallet B., et al. Sevoflurane pre- and post-conditioning protect the brain via the mitochondrial K ATP channel. Br J Anaesth 2010, 104:191-200.
2. Ben Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 2002, 3:728-739.
3. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 1993, 361:315-325.
4. 2+-dependent survival signaling in cortical neurons and modulates MAP kinases, apoptosis proteins and transcription factors during hypoxia. Anesth Analg 2006, 103:419-429.
5. 2+ and mitogen-activated protein kinase signaling. Anesthesiology 2005, 103:532-539.
6. Bloomfield S.M., McKinney J., Smith L., Brisman J. Reliability of S100B in predicting severity of central nervous system injury. Neurocrit Care 2007, 6:121-138.
7. Cai J., Hu Y., Li W., Li L., Li S., Zhang M., et al. The neuroprotective effect of propofol against brain ischemia mediated by the glutamatergic signaling pathway in rats. Neurochem Res 2011, 36:1724-1731.
8. 2+ transfer to mitochondria. Cell 2010, 142:270-283.
9. Chakroborty S., Goussakov I., Miller M.B., Stutzmann G.E. Deviant ryanodine receptor-mediated calcium release resets synaptic homeostasis in presymptomatic 3xTg-AD mice. J Neurosci 2009, 29:9458-9470.
10. Culley D.J., Baxter M., Yukhananov R., Crosby G. The memory effects of general anesthesia persist for weeks in young and aged rats. Anesth Analg 2003, 96:1004-1009.
11. Decuypere J.P., Monaco G., Bultynck G., Missiaen L., De S.H., Parys J.B. The IP(3) receptor-mitochondria connection in apoptosis and autophagy. Biochim Biophys Acta 2011, 1813:1003-1013.
12. Dickinson R., Peterson B.K., Banks P., Simillis C., Martin J.C., Valenzuela C.A., 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, 107:756-767.
13. Eberspacher E., Eckel B., Engelhard K., Muller K., Hoffman W.E., Blobner M., et al. Effects of sevoflurane on cognitive deficit, motor function, and histopathology after cerebral ischemia in rats. Acta Anaesthesiol Scand 2009, 53:774-782.
14. Feng J., Zuo Z. Isoflurane preconditioning increases endothelial cell tolerance to in-vitro simulated ischaemia. J Pharm Pharmacol 2011, 63:106-110.
15. Franks N.P. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 2008, 9:370-386.
16. Garaschuk O., Hanse E., Konnerth A. Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol 1998, 507(Pt 1):219-236.
17. 2+ and mitogen-activated protein kinases. Anesthesiology 2005, 102(3):606-615.
18. Green D.R., Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004, 305:626-629.
19. Hajnoczky G., Davies E., Madesh M. Calcium signaling and apoptosis. Biochem Biophys Res Commun 2003, 304(3):445-454. [[Review] [93 refs]].
20. Hanson C.J., Bootman M.D., Roderick H.L. Cell signalling: IP3 receptors channel calcium into cell death. Curr Biol 2004, 14:R933-R935.
21. Ikonomidou C., Bittigau P., Koch C., Genz K., Hoerster F., Felderhoff-Mueser U., et al. Neurotransmitters and apoptosis in the developing brain. Biochem Pharmacol 2001, 62:401-405.
22. Inan S., Wei H. The cytoprotective effects of dantrolene: a ryanodine receptor antagonist. Anesth Analg 2010, 111:1400-1410.
23. Istaphanous G.K., Howard J., Nan X., Hughes E.A., Mccann J.C., McAuliffe J.J., et al. Comparison of the neuroapoptotic properties of equipotent anesthetic concentrations of desflurane, isoflurane, or sevoflurane in neonatal mice. Anesthesiology 2011, 114:578-587.
24. Jevtovic-Todorovic V., Carter L.B. The anesthetics nitrous oxide and ketamine are more neurotoxic to old than to young rat brain. Neurobiol Dis 2005, 26:947-956.
25. Jevtovic-Todorovic V., Hartman R.E., Izumi Y., Benshoff N.D., Dikranian K., Zorumski C.F., et al. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003, 23:876-882.
26. Kalkman C.J., Peelen L., Moons K.G., Veenhuizen M., Bruens M., Sinnema G., et al. Behavior and development in children and age at the time of first anesthetic exposure. Anesthesiology 2009, 110:805-812.
27. Kawaguchi M., Furuya H., Patel P.M. Neuroprotective effects of anesthetic agents. J Anesth 2005, 19:150-156.
28. Korge P., Honda H.M., Weiss J.N. Protection of cardiac mitochondria by diazoxide and protein kinase C: implications for ischemic preconditioning. Proc Natl Acad Sci U S A 2002, 99:3312-3317.
29. Kudo M., Aono M., Lee Y., Massey G., Pearlstein R.D., Warner D.S. Effects of volatile anesthetics on N-methyl-D-aspartate excitotoxicity in primary rat neuronal-glial cultures. Anesthesiology 2001, 95:756-765.
30. Kvolik S., Glavas-Obrovac L., Bares V., Karner I. Effects of inhalation anesthetics halothane, sevoflurane, and isoflurane on human cell lines. Life Sci 2005, 77:2369-2383.
31. Li L., Zuo Z. Isoflurane preconditioning improves short-term and long-term neurological outcome after focal brain ischemia in adult rats. Neuroscience 2009, 164:497-506.
32. Li Y., Liang G., Wang S., Meng Q., Wang Q., Wei H. Effect of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology 2007, 53:942-950.
33. Liang G., Wang Q.J., Li Y., Kang B., Eckenhoff M.F., Eckenhoff R.G., et al. A presenilin-1 mutation renders neurons vulnerable to isoflurane toxicity. Anesth Analg 2008, 106:492-500.
34. Liang G., Ward C., Peng J., Zhao Y., Huang B., Wei H. Isoflurane causes greater neurodegeneration than an equivalent exposure of sevoflurane in the developing brain of neonatal mice. Anesthesiology 2010, 112:1325-1334.
35. Lin D., Li G., Zuo Z. Volatile anesthetic post-treatment induces protection via inhibition of glycogen synthase kinase 3beta in human neuron-like cells. Neuroscience 2011, 179:73-79.
36. Ma D., Williamson P., Januszewski A., Nogaro M.C., Hossain M., Ong L.P., et al. Xenon mitigates isoflurane-induced neuronal apoptosis in the developing rodent brain. Anesthesiology 2007, 106:746-753.
37. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003, 4:552-565.
38. Pan C., Xu Z., Dong Y., Zhang Y., Zhang J., McAuliffe S., et al. The potential dual effects of anesthetic isoflurane on hypoxia-induced caspase-3 activation and increases in beta-site amyloid precursor protein-cleaving enzyme levels. Anesth Analg 2011, 113:145-152.
39. Peng Y., Cheung K.H., Foskett J., Li J., Wei H. Isoflurane activates inositol 1,4,5-trisphosphate receptors. Program # 818.11/C4. 2009 Neuroscience Meeting Planner 2009, Society for Neuroscience, Chicago, IL, [Online].
40. Peng J., Inan S., Liang G., Wei H. Preconditioning with isoflurane prevents prolonged exposure of isoflurane-induced apoptosis in developing rat brains. Program No. 157.6/Q5. 2010 Neuroscience Meeting Planner 2010, Society for Neuroscience, San Diego, CA, [Online].
41. Peng Y., Fosket K., Vais H., Joseph D., Liang G., Wei H. The general anesthetics facilitate activation of inositol 1,4,5-trisphosphate (InsP3) receptors. Neuroscience Meeting Planner 2012, Society for Neuroscience, Washington, DC, [Online, 2011].
42. Popovic R., Liniger R., Bickler P.E. Anesthetics and mild hypothermia similarly prevent hippocampal neuron death in an in vitro model of cerebral ischemia. Anesthesiology 2000, 92:1343-1349.
43. Rammes G., Starker L.K., Haseneder R., Berkmann J., Plack A., Zieglgansberger W., et al. Isoflurane anaesthesia reversibly improves cognitive function and long-term potentiation (LTP) via an up-regulation in NMDA receptor 2B subunit expression. Neuropharmacology 2009, 56:626-636.
44. 2+ from the endoplasmic reticulum to mitochondria: is spatial intimacy enough?. Biochem Soc Trans 2006, 34:351-355.
45. Sakai H., Sheng H., Yates R.B., Ishida K., Pearlstein R.D., Warner D.S. Isoflurane provides long-term protection against focal cerebral ischemia in the rat. Anesthesiology 2007, 106:92-99.
46. Sanders R.D., Xu J., Shu Y., Januszewski A., Halder S., Fidalgo A., et al. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats. Anesthesiology 2009, 110:1077-1085.
47. Shu Y., Patel S.M., Pac-Soo C., Fidalgo A.R., Wan Y., Maze M., et al. Xenon pretreatment attenuates anesthetic-induced apoptosis in the developing brain in comparison with nitrous oxide and hypoxia. Anesthesiology 2010, 113:360-368.
48. Shu Y., Zhou Z., Wan Y., Sanders R.D., Li M., Pac-Soo C.K., et al. Nociceptive stimuli enhance anesthetic-induced neuroapoptosis in the rat developing brain. Neurobiol Dis 2012, 45:743-750.
49. 2+ oscillations. Anesth Analg 2011, 113:1161-1169.
50. 2+-oscillations. Toxicology 2011, 290:96-101.
51. Slikker W., Zou X.J., Hotchkiss C.E., Divine R.L., Sadovova N., Twaddle N.C., et al. Ketamine-induced neuronal cell death in the perinatal rhesus monkey. Toxicol Sci 2007, 98:145-158.
52. Slow E.J., van Raamsdonk J., Rogers D., Coleman S.H., Graham R.K., Deng Y., et al. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 2003, 12:1555-1567.
53. Soriano S.G., Liu Q., Li J., Liu J.R., Han X.H., Kanter J.L., et al. Ketamine activates cell cycle signaling and apoptosis in the neonatal rat brain. Anesthesiology 2010, 112:1155-1163.
54. Stratmann G., May L.D.V., Sall J.W., Alvi R.S., Bell J.S., Ormerod B.K., et al. Effect of hypercarbia and isoflurane on brain cell death and neurocognitive dysfunction in 7-day-old rats. Anesthesiology 2009, 110:849-861.
55. Takadera T., Ishida A., Ohyashiki T. Ketamine-induced apoptosis in cultured rat cortical neurons. Toxicol Appl Pharmacol 2006, 210(1-2):100-107.
56. Tanaka K., Ludwig L.M., Kersten J.R., Pagel P.S., Warltier D.C. Mechanisms of cardioprotection by volatile anesthetics. Anesthesiology 2004, 100:707-721.
57. Wang S., Peretich K., Zhao Y., Liang G., Meng Q., Wei H. Anesthesia-induced neurodegeneration in fetal rat brains. Pediatr Res 2009, 66:435-440.
58. Wang J.K., Yu L.N., Zhang F.J., Yang M.J., Yu J., Yan M., et al. Postconditioning with sevoflurane protects against focal cerebral ischemia and reperfusion injury via PI3K/Akt pathway. Brain Res 2010, 1357:142-151.
59. Wang Q., Liang G., Yang H., Wang S., Eckenhoff M.F., Wei H. The common inhaled anesthetic isoflurane increases aggregation of huntingtin and alters calcium homeostasis in a cell model of Huntington's disease. Toxicol Appl Pharmacol 2011, 250:291-298.
60. Wei H. The role of calcium dysregulation in anesthetic-mediated neurotoxicity. Anesth Analg 2011, 113:972-974.
61. Wei H., Xie Z. Anesthesia, calcium homeostasis and Alzheimer's disease. Curr Alzheimer Res 2009, 6:30-35.
62. Wei H., Kang B., Wei W., Liang G., Meng Q.C., Li Y., et al. Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Res 2005, 1037:139-147.
63. Wei H., Liang G., Yang H. Isoflurane preconditioning inhibited isoflurane-induced neurotoxicity. Neurosci Lett 2007, 425:59-62.
64. Wei H.F., Liang G., Yang H., Wang Q.J., Hawkins B., Madesh M., et al. The common inhalational anesthetic isoflurane induces apoptosis via activation of inositol 1,4,5-trisphosphate receptors. Anesthesiology 2008, 108:251-260.
65. Wilder R.T., Flick R.P., Sprung J., Katusic S.K., Barbaresi W.J., Mickelson C., et al. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 2009, 110:796-804.
66. Wu G.J., Chen W.F., Hung H.C., Jean Y.H., Sung C.S., Chakraborty C., et al. Effects of propofol on proliferation and anti-apoptosis of neuroblastoma SH-SY5Y cell line: new insights into neuroprotection. Brain Res 2011, 1384:42-50.
67. Xiang Q., Tan L., Zhao Y.L., Wang J.T., Jin X.G., Luo A.L. Isoflurane enhances spontaneous Ca(2+) oscillations in developing rat hippocampal neurons in vitro. Acta Anaesthesiol Scand 2009, 53:765-773.
68. Xu Z., Dong Y., Wu X., Zhang J., McAuliffe S., Pan C., et al. The potential dual effects of anesthetic isoflurane on Abeta-induced apoptosis. Curr Alzheimer Res 2011, 8:741-752.
69. Yang H., Liang G., Hawkins B.J., Madesh M., Pierwola A., Wei H.F. Inhalational anesthetics induce cell damage by disruption of intracellular calcium homeostasis with different potencies. Anesthesiology 2008, 109:243-250.
70. Zhao P., Zuo Z. Isoflurane preconditioning induces neuroprotection that is inducible nitric oxide synthase-dependent in neonatal rats. Anesthesiology 2004, 101(3):695-703.
71. Zhao Y., Liang G., Chen Q., Joseph D.J., Meng Q., Eckenhoff R.G., et al. Anesthetic-induced neurodegeneration mediated via inositol 1,4,5-trisphosphate receptors. J Pharmacol Exp Ther 2010, 333:14-22.
72. Zhao Y.L., Xiang Q., Shi Q.Y., Li S.Y., Tan L., Wang J.T., et al. GABAergic excitotoxicity injury of the immature hippocampal pyramidal neurons' exposure to isoflurane. Anesth Analg 2011, 113:1152-1160.
73. Zhao X., Yang Z., Liang G., Wu Z., Peng Y., Joseph D.J., et al. Dual effects of isoflurane on proliferation, differentiation, and survival in human neuroprogenitor cells. Anesthesiology 2013, 118:537-549.
74. Zheng S., Zuo Z. Isoflurane preconditioning induces neuroprotection against ischemia via activation of P38 mitogen-activated protein kinases. Mol Pharmacol 2004, 65(5):1172-1180.
75. Zheng S., Zuo Z. Isoflurane preconditioning decreases glutamate receptor overactivation-induced Purkinje neuronal injury in rat cerebellar slices. Brain Res 2005, 1054(2):143-151.
76. Zhou Y., Lekic T., Fathali N., Ostrowski R.P., Martin R.D., Tang J., et al. Isoflurane posttreatment reduces neonatal hypoxic-ischemic brain injury in rats by the sphingosine-1-phosphate/phosphatidylinositol-3-kinase/Akt pathway. Stroke 2010, 41:1521-1527.