Isoflurane but not sevoflurane or desflurane aggravates injury to neurons in vitro and in vivo via p75NTR-NF-κB Activation

Anesthesia and Analgesia

Volumn 119, Issue 6, 2014, Pages 1429-1441

  Schallner, Nils ^a   Ulbrich, Felix ^a   Engelstaedter, Helen ^a   Biermann, Julia ^b   Auwaerter, Volker ^a   Loop, Torsten ^a   Goebel, Ulrich ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DESFLURANE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOFLURANE; LACTATE DEHYDROGENASE; NEUROTROPHIN RECEPTOR P75; SEVOFLURANE; SMALL INTERFERING RNA; ETHER DERIVATIVE; GLUCOSE; INHALATION ANESTHETIC AGENT; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NGFR PROTEIN, HUMAN; PEPTIDE FRAGMENT; TNFRSF16 PROTEIN, RAT; TRANSACTIVATOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BIOLUMINESCENCE; CELL DAMAGE; CELL DENSITY; CONTROLLED STUDY; CULTURE MEDIUM; DEPOLARIZATION; DNA BINDING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MALE; MASS FRAGMENTOGRAPHY; MINIMUM LUNG ALVEOLUS CONCENTRATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OPTICAL DENSITY; PROTEIN PHOSPHORYLATION; RAT; REOXYGENATION; REPERFUSION INJURY; RETINA GANGLION CELL; RNA INTERFERENCE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL DEATH; CELL HYPOXIA; CHEMICALLY INDUCED; COMPARATIVE STUDY; DEFICIENCY; DOSE RESPONSE; DRUG EFFECTS; GENETIC TRANSFECTION; HUMAN; METABOLISM; NERVE CELL; PATHOLOGY; PROMOTER REGION; RETINA DISEASE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TOXICITY; TUMOR CELL LINE;

ANESTHETICS, INHALATION; ANIMALS; BINDING SITES; CELL DEATH; CELL HYPOXIA; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUCOSE; HUMANS; ISOFLURANE; MALE; METHYL ETHERS; NERVE TISSUE PROTEINS; NEURONS; NF-KAPPA B; PEPTIDE FRAGMENTS; PROMOTER REGIONS, GENETIC; RATS, SPRAGUE-DAWLEY; RECEPTORS, NERVE GROWTH FACTOR; REPERFUSION INJURY; RETINAL DISEASES; RETINAL GANGLION CELLS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSFECTION;

EID: 84914094764     PISSN: 00032999     EISSN: 15267598     Source Type: Journal    
DOI: 10.1213/ANE.0000000000000488     Document Type: Article

References (68)

1. 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
2. Lee JJ, Li L, Jung HH, Zuo Z. Postconditioning with isoflurane reduced ischemia-induced brain injury in rats. Anesthesiology 2008;108:1055-62
3. Zhou Y, Lekic T, Fathali N, Ostrowski RP, Martin RD, Tang J, Zhang JH. Isoflurane posttreatment reduces neonatal hypoxicischemic brain injury in rats by the sphingosine-1-phosphate/phosphatidylinositol-3-kinase/Akt pathway. Stroke 2010;41:1521-7
4. Hu Q, Ma Q, Zhan Y, He Z, Tang J, Zhou C, Zhang J. Isoflurane enhanced hemorrhagic transformation by impairing antioxidant enzymes in hyperglycemic rats with middle cerebral artery occlusion. Stroke 2011;42:1750-6
5. Jiang H, Huang Y, Xu H, Sun Y, Han N, Li QF. Hypoxia inducible factor-1α is involved in the neurodegeneration induced by isoflurane in the brain of neonatal rats. J Neurochem 2012;120:453-60
6. Wei H, Liang G, Yang H, Wang Q, Hawkins B, Madesh M, Wang S, Eckenhoff RG. The common inhalational anesthetic isoflurane induces apoptosis via activation of inositol 1,4,5-trisphosphate receptors. Anesthesiology 2008;108:251-60
7. Zhu C, Gao J, Karlsson N, Li Q, Zhang Y, Huang Z, Li H, Kuhn HG, Blomgren K. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab 2010;30:1017-30
8. Brosnan H, Bickler PE. Xenon neurotoxicity in rat hippocampal slice cultures is similar to isoflurane and sevoflurane. Anesthesiology 2013;119:335-44
9. Murphy KL, Baxter MG. Long-term effects of neonatal single or multiple isoflurane exposures on spatial memory in rats. Front Neurol 2013;4:87
10. Zhao X, Yang Z, Liang G, Wu Z, Peng Y, Joseph DJ, Inan S, Wei H. Dual effects of isoflurane on proliferation, differentiation, and survival in human neuroprogenitor cells. Anesthesiology 2013;118:537-49
11. Adamczyk S, Robin E, Simerabet M, Kipnis E, Tavernier B, Vallet B, Bordet R, Lebuffe G. Sevoflurane pre- and post-conditioning protect the brain via the mitochondrial K ATP channel. Br J Anaesth 2010;104:191-200
12. Lu Y, Wu X, Dong Y, Xu Z, Zhang Y, Xie Z. Anesthetic sevoflurane causes neurotoxicity differently in neonatal nave and Alzheimer disease transgenic mice. Anesthesiology 2010;112:1404-16
13. Zheng H, Dong Y, Xu Z, Crosby G, Culley DJ, Zhang Y, Xie Z. Sevoflurane anesthesia in pregnant mice induces neurotoxicity in fetal and offspring mice. Anesthesiology 2013;118:516-26
14. McAuliffe JJ, Loepke AW, Miles L, Joseph B, Hughes E, Vorhees CV. Desflurane, isoflurane, and sevoflurane provide limited neuroprotection against neonatal hypoxia-ischemia in a delayed preconditioning paradigm. Anesthesiology 2009;111:533-46
15. Istaphanous GK, Howard J, Nan X, Hughes EA, McCann JC, McAuliffe JJ, Danzer SC, Loepke AW. Comparison of the neuroapoptotic properties of equipotent anesthetic concentrations of desflurane, isoflurane, or sevoflurane in neonatal mice. Anesthesiology 2011;114:578-87
16. Haelewyn B, Yvon A, Hanouz JL, MacKenzie ET, Ducouret P, Gérard JL, Roussel S. Desflurane affords greater protection than halothane against focal cerebral ischaemia in the rat. Br J Anaesth 2003;91:390-6
17. Bedirli N, Bagriacik EU, Emmez H, Yilmaz G, Unal Y, Ozkose Z. Sevoflurane and isoflurane preconditioning provides neuroprotection by inhibition of apoptosis-related mRNA expression in a rat model of focal cerebral ischemia. J Neurosurg Anesthesiol 2012;24:336-44
18. Lemkuil BP, Head BP, Pearn ML, Patel HH, Drummond JC, Patel PM. Isoflurane neurotoxicity is mediated by p75NTRRhoA activation and actin depolymerization. Anesthesiology 2011;114:49-57
19. Head BP, Patel HH, Niesman IR, Drummond JC, Roth DM, Patel PM. Inhibition of p75 neurotrophin receptor attenuates isoflurane-mediated neuronal apoptosis in the neonatal central nervous system. Anesthesiology 2009;110:813-25
20. Pearn ML, Hu Y, Niesman IR, Patel HH, Drummond JC, Roth DM, Akassoglou K, Patel PM, Head BP. Propofol neurotoxicity is mediated by p75 neurotrophin receptor activation. Anesthesiology 2012;116:352-61
21. Schulte JH, Pentek F, Hartmann W, Schramm A, Friedrichs N, ra I, Koster J, Versteeg R, Kirfel J, Buettner R, Eggert A. The low-affinity neurotrophin receptor, p75, is upregulated in ganglioneuroblastoma/ganglioneuroma and reduces tumorigenicity of neuroblastoma cells in vivo. Int J Cancer 2009;124:2488-94
22. Sun Y, Lim Y, Li F, Liu S, Lu JJ, Haberberger R, Zhong JH, Zhou XF. ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PLoS One 2012;7:e35883
23. Park KJ, Grosso CA, Aubert I, Kaplan DR, Miller FD. p75NTRdependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat Neurosci 2010;13:559-66
24. Lebrun-Julien F, Bertrand MJ, De Backer O, Stellwagen D, Morales CR, Di Polo A, Barker PA. ProNGF induces TNFalphadependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc Natl Acad Sci U S A 2010;107:3817-22
25. Kenchappa RS, Tep C, Korade Z, Urra S, Bronfman FC, Yoon SO, Carter BD. p75 neurotrophin receptor-mediated apoptosis in sympathetic neurons involves a biphasic activation of JNK and up-regulation of tumor necrosis factor-alpha-converting enzyme/ADAM17. J Biol Chem 2010;285:20358-68
26. Greferath U, Mallard C, Roufail E, Rees SM, Barrett GL, Bartlett PF. Expression of the p75 neurotrophin receptor by striatal cholinergic neurons following global ischemia in rats is associated with neuronal degeneration. Neurosci Lett 2002;332:57-60
27. Wei Y, Wang N, Lu Q, Zhang N, Zheng D, Li J. Enhanced protein expressions of sortilin and p75NTR in retina of rat following elevated intraocular pressure-induced retinal ischemia. Neurosci Lett 2007;429:169-74
28. Park JA, Lee JY, Sato TA, Koh JY. Co-induction of p75NTR and p75NTR-associated death executor in neurons after zinc exposure in cortical culture or transient ischemia in the rat. J Neurosci 2000;20:9096-103
29. Bai Y, Li Q, Yang J, Zhou X, Yin X, Zhao D. p75(NTR) activation of NF-kappaB is involved in PrP106-126-induced apoptosis in mouse neuroblastoma cells. Neurosci Res 2008;62:9-14
30. Costantini C, Rossi F, Formaggio E, Bernardoni R, Cecconi D, Della-Bianca V. Characterization of the signaling pathway downstream p75 neurotrophin receptor involved in beta-amyloid peptide-dependent cell death. J Mol Neurosci 2005;25:141-56
31. Kuner P, Schubenel R, Hertel C. Beta-amyloid binds to p57NTR and activates NFkappaB in human neuroblastoma cells. J Neurosci Res 1998;54:798-804
32. Peters FT HM, Herbold M, Schmitt G, Daldrup T, Muhoff F. Anhang B zu den Richtlinien der GTFCh zur Qualittssicherung bei forensisch-toxikologischen Untersuchungen; Anforderungen an die Validierung von Analysenmethoden. Toxichem Krimtech 2009;76:185 (German)
33. Schallner N, Romo CC, Biermann J, Lagrze WA, Otterbein LE, Buerkle H, Loop T, Goebel U. Carbon monoxide abrogates ischemic insult to neuronal cells via the soluble guanylate cyclase-cGMP pathway. PLoS One 2013;8:e60672
34. Schallner N, Fuchs M, Schwer CI, Loop T, Buerkle H, Lagrze WA, van Oterendorp C, Biermann J, Goebel U. Postconditioning with inhaled carbon monoxide counteracts apoptosis and neuroinflammation in the ischemic rat retina. PLoS One 2012;7:e46479
35. Fischer D, Pavlidis M, Thanos S. Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest Ophthalmol Vis Sci 2000;41:3943-54
36. Biermann J, Lagrze WA, Schallner N, Schwer CI, Goebel U. Inhalative preconditioning with hydrogen sulfide attenuated apoptosis after retinal ischemia/reperfusion injury. Mol Vis 2011;17:1275-86
37. Franks NP, Lieb WR. Temperature dependence of the potency of volatile general anesthetics: implications for in vitro experiments. Anesthesiology 1996;84:716-20
38. Strum DP, Eger EI 2nd. Partition coefficients for sevoflurane in human blood, saline, and olive oil. Anesth Analg 1987;66:654-6
39. Zhao YL, Xiang Q, Shi QY, Li SY, Tan L, Wang JT, Jin XG, Luo AL. GABAergic excitotoxicity injury of the immature hippocampal pyramidal neurons exposure to isoflurane. Anesth Analg 2011;113:1152-60
40. Wang WY, Luo Y, Jia LJ, Hu SF, Lou XK, Shen SL, Lu H, Zhang HH, Yang R, Wang H, Ma ZW, Xue QS, Yu BW. Inhibition of aberrant cyclin-dependent kinase 5 activity attenuates isoflurane neurotoxicity in the developing brain. Neuropharmacology 2014;77:90-9
41. Ma D, Williamson P, Januszewski A, Nogaro MC, Hossain M, Ong LP, Shu Y, Franks NP, Maze M. Xenon mitigates isofluraneinduced neuronal apoptosis in the developing rodent brain. Anesthesiology 2007;106:746-53
42. Zhen Y, Dong Y, Wu X, Xu Z, Lu Y, Zhang Y, Norton D, Tian M, Li S, Xie Z. Nitrous oxide plus isoflurane induces apoptosis and increases beta-amyloid protein levels. Anesthesiology 2009;111:741-52
43. Zhang J, Dong Y, Xu Z, Zhang Y, Pan C, McAuliffe S, Ichinose F, Yue Y, Liang W, Xie Z. 2-Deoxy-D-glucose attenuates isoflurane- induced cytotoxicity in an in vitro cell culture model of H4 human neuroglioma cells. Anesth Analg 2011;113:1468-75
44. Pan C, Xu Z, Dong Y, Zhang Y, Zhang J, McAuliffe S, Yue Y, Li T, Xie Z. The potential dual effects of anesthetic isoflurane on hypoxia-induced caspase-3 activation and increases in β-site amyloid precursor protein-cleaving enzyme levels. Anesth Analg 2011;113:145-52
45. Cao L, Feng C, Li L, Zuo Z. Contribution of microRNA-203 to the isoflurane preconditioning-induced neuroprotection. Brain Res Bull 2012;88:525-8
46. Gwak MS, Cao L, Li L, Zuo Z. Isoflurane preconditioning reduces oxygen-glucose deprivation-induced neuronal injury via B-cell lymphoma 2 protein. Environ Toxicol Pharmacol 2011;31:262-5
47. Zhao XC, Zhang LM, Li Q, Tong DY, Fan LC, An P, Wu XY, Chen WM, Zhao P, Wang J. Isoflurane post-conditioning protects primary cultures of cortical neurons against oxygen and glucose deprivation injury via upregulation of Slit2/Robo1. Brain Res 2013;1537:283-9
48. Wu GJ, Chen WF, Sung CS, Jean YH, Hung CH, Chen FA, Hsieh MH, Wen ZH. Isoflurane attenuates dynorphin-induced cytotoxicity and downregulation of Bcl-2 expression in differentiated neuroblastoma SH-SY5Y cells. Acta Anaesthesiol Scand 2009;53:55-60
49. Li H, Yin J, Li L, Deng J, Feng C, Zuo Z. Isoflurane postconditioning reduces ischemia-induced nuclear factor-κB activation and interleukin 1β production to provide neuroprotection in rats and mice. Neurobiol Dis 2013;54:216-24
50. McMurtrey RJ, Zuo Z. Isoflurane preconditioning and postconditioning in rat hippocampal neurons. Brain Res 2010;1358:184-90
51. Sakai H, Sheng H, Yates RB, Ishida K, Pearlstein RD, Warner DS. Isoflurane provides long-term protection against focal cerebral ischemia in the rat. Anesthesiology 2007;106:92-9
52. Zhao P, Peng L, Li L, Xu X, Zuo Z. Isoflurane preconditioning improves long-term neurologic outcome after hypoxic-ischemic brain injury in neonatal rats. Anesthesiology 2007;107:963-70
53. Ye R, Yang Q, Kong X, Li N, Zhang Y, Han J, Xiong L, Liu X, Zhao G. Sevoflurane preconditioning improves mitochondrial function and long-term neurologic sequelae after transient cerebral ischemia: role of mitochondrial permeability transition. Crit Care Med 2012;40:2685-93
54. Ye Z, Guo Q, Xia P, Wang N, Wang E, Yuan Y. Sevoflurane postconditioning involves an up-regulation of HIF-1α and HO-1 expression via PI3K/Akt pathway in a rat model of focal cerebral ischemia. Brain Res 2012;1463:63-74
55. Velly LJ, Canas PT, Guillet BA, Labrande CN, Masmejean FM, Nieoullon AL, Gouin FM, Bruder NJ, Pisano PS. Early anesthetic preconditioning in mixed cortical neuronal-glial cell cultures subjected to oxygen-glucose deprivation: the role of adenosine triphosphate dependent potassium channels and reactive oxygen species in sevoflurane-induced neuroprotection. Anesth Analg 2009;108:955-63
56. Wang WY, Wang H, Luo Y, Jia LJ, Zhao JN, Zhang HH, Ma ZW, Xue QS, Yu BW. The effects of metabotropic glutamate receptor 7 allosteric agonist N,N-dibenzhydrylethane-1,2-diamine dihydrochloride on developmental sevoflurane neurotoxicity: role of extracellular signal-regulated kinase 1 and 2 mitogenactivated protein kinase signaling pathway. Neuroscience 2012;205:167-77
57. Wang QJ, Li KZ, Yao SL, Li ZH, Liu SS. Different effects of isoflurane and sevoflurane on cytotoxicity. Chin Med J (Engl) 2008;121:341-6
58. Caas N, Valero T, Villarroya M, Montell E, Vergés J, García AG, López MG. Chondroitin sulfate protects SH-SY5Y cells from oxidative stress by inducing heme oxygenase-1 via phosphatidylinositol 3-kinase/Akt. J Pharmacol Exp Ther 2007;323:946-53
59. Xiong N, Jia M, Chen C, Xiong J, Zhang Z, Huang J, Hou L, Yang H, Cao X, Liang Z, Sun S, Lin Z, Wang T. Potential autophagy enhancers attenuate rotenone-induced toxicity in SH-SY5Y. Neuroscience 2011;199:292-302
60. Newhouse K, Hsuan SL, Chang SH, Cai B, Wang Y, Xia Z. Rotenone-induced apoptosis is mediated by p38 and JNK MAP kinases in human dopaminergic SH-SY5Y cells. Toxicol Sci 2004;79:137-46
61. Zuo Z, Wang Y, Huang Y. Isoflurane preconditioning protects human neuroblastoma SH-SY5Y cells against in vitro simulated ischemia-reperfusion through the activation of extracellular signal-regulated kinases pathway. Eur J Pharmacol 2006;542:84-91
62. Bono F, Lamarche I, Bornia J, Savi P, Della Valle G, Herbert JM. Nerve growth factor (NGF) exerts its pro-apoptotic effect via the P75NTR receptor in a cell cycle-dependent manner. FEBS Lett 1999;457:93-7
63. Li SY, Yang D, Yeung CM, Yu WY, Chang RC, So KF, Wong D, Lo AC. Lycium barbarum polysaccharides reduce neuronal damage, blood-retinal barrier disruption and oxidative stress in retinal ischemia/reperfusion injury. PLoS One 2011;6:e16380
64. Zhang Z, Qin X, Tong N, Zhao X, Gong Y, Shi Y, Wu X. Valproic acid-mediated neuroprotection in retinal ischemia injury via histone deacetylase inhibition and transcriptional activation. Exp Eye Res 2012;94:98-108
65. Yamashita T, Tohyama M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 2003;6:461-7
66. Ferlisi M, Shorvon S. The outcome of therapies in refractory and super-refractory convulsive status epilepticus and recommendations for therapy. Brain 2012;135:2314-28
67. Villa F, Iacca C, Molinari AF, Giussani C, Aletti G, Pesenti A, Citerio G. Inhalation versus endovenous sedation in subarachnoid hemorrhage patients: effects on regional cerebral blood flow. Crit Care Med 2012;40:2797-804
68. Fugate JE, Burns JD, Wijdicks EF, Warner DO, Jankowski CJ, Rabinstein AA. Prolonged high-dose isoflurane for refractory status epilepticus: is it safe? Anesth Analg 2010;111:1520-4