In vitro induction of endothelial apoptosis of the post-hypoxic blood-brain barrier by isoflurane but not by sevoflurane and midazolam

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Dittmar, Michael S ^a   Petermichl, Walter ^a   Lindner, Regina ^a   Sinner, Barbara ^a   Graf, Bernhard M ^a   Schlachetzki, Felix ^a   Gruber, Michael ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ISOFLURANE; MIDAZOLAM; PROTEIN BAX; PROTEIN BCL 2; SEVOFLURANE; ETHER DERIVATIVE;

APOPTOSIS; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL HYPOXIA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; REOXYGENATION; RISK ASSESSMENT; RISK FACTOR; TUNEL ASSAY; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; DRUG EFFECTS; METABOLISM;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOOD-BRAIN BARRIER; CELL HYPOXIA; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOFLURANE; METHYL ETHERS; MIDAZOLAM; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84939245885     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130408     Document Type: Article

References (40)

1. Zhang Y, Zhang F, Meng C, Tian S, Wang Y, Zhao W, et al. Inhibition of Sevoflurane Postconditioning Against Cerebral Ischemia Reperfusion-Induced Oxidative Injury in Rats. Molecules 2012; 17: 341-354.
2. Altay O, Suzuki H, Hasegawa Y, Caner B, Krafft PR, Fujii M, et al. Isoflurane Attenuates Blood-Brain Barrier Disruption in Ipsilateral Hemisphere After Subarachnoid Hemorrhage in Mice. Stroke 2012; 43: 2513-2516. doi: 10.1161/STROKEAHA.112.661728 PMID: 22773559
3. 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: 336-344. doi: 10.1097/ANA.0b013e318266791e PMID: 22871953
4. Engelhard K, Werner C, Reeker W, Lu H, Mollenberg O, Mielke L, et al. Desflurane and isoflurane improve neurological outcome after incomplete cerebral ischaemia in rats. Br J Anaesth. 1999; 83: 415-421. PMID: 10655912
5. Gwak M, 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: 262-265. doi: 10.1016/j.etap.2010.10.009 PMID: 21359097
6. Ren X, Wang Z, Ma H, Zuo Z. Sevoflurane postconditioning provides neuroprotection against brain hypoxia - ischemia in neonatal rats. Neurol Sci. 2014; 35: 1401-1404. doi: 10.1007/s10072-014-1726-4 PMID: 24705859
7. Taheri S, Shunmugavel A, Clark D, Shi H. Isoflurane reduces the ischemia reperfusion injury surge: A longitudinal study with MRI. Brain Res. 2014; 1586: 173-183. doi: 10.1016/j.brainres.2014.08.003 PMID: 25124744
8. Wang J, Yu L, Zhang F, Yang M, 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. doi: 10.1016/j.brainres.2010.08.009 PMID: 20705063
9. Zhou Y, Lekic T, Fathali N, Ostrowski RP, Martin RD, 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. doi: 10.1161/STROKEAHA.110.583757 PMID: 20508187
10. 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. doi: 10.1097/ALN.0b013e3181d94da5 PMID: 20460994
11. Loepke AW, Istaphanous GK, McAuliffe JJ, Miles L, Hughes EA, McCann JC, et al. The Effects of Neonatal Isoflurane Exposure in Mice on Brain Cell Viability, Adult Behavior, Learning, and Memory. Anesth Analg. 2009; 108: 90-104. doi: 10.1213/ane.0b013e31818cdb29 PMID: 19095836
12. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski C, 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. PMID: 12574416
13. Yon J, Daniel-Johnson J, Carter LB, Jevtovic-Todorovic V. Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience 2005; 135: 815-827. PMID: 16154281
14. Zheng H, Dong Y, Xu Z, Crosby G, Culley DJ, Zhang Y, et al. Sevoflurane anesthesia in pregnant mice induces neurotoxicity in fetal and offspring mice. Anesthesiology 2013; 118: 516-526. doi: 10.1097/ALN.0b013e3182834d5d PMID: 23314109
15. Sinner B, Friedrich O, Zausig Y, Bein T, Graf BM. Toxic effects of midazolam on differentiating neurons in vitro as a consequence of suppressed neuronal Ca2+-oscillations. Toxicology 2011; 290: 96-101. doi: 10.1016/j.tox.2011.08.022 PMID: 21920406
16. Hu Q, Ma Q, Zhan Y, He Z, Tang J, Zhou C, et al. Isoflurane Enhanced Hemorrhagic Transformation by Impairing Antioxidant Enzymes in Hyperglycemic Rats With Middle Cerebral Artery Occlusion. Stroke 2011; 42: 1750-1756. doi: 10.1161/STROKEAHA.110.603142 PMID: 21474807
17. Hertle D, Beynon C, Zweckberger K, Vienenkötter B, Jung CS, Kiening K, et al. Influence of isoflurane on neuronal death and outcome in a rat model of traumatic brain injury. Acta Neurochir Suppl. 2012; 114: 383-386. doi: 10.1007/978-3-7091-0956-4-74 PMID: 22327728
18. Dittmar MS, Petermichl W, Schlachetzki F, Graf BM, Gruber M. Isoflurane Induces Endothelial Apoptosis of the Post-Hypoxic Blood-Brain Barrier in a Transdifferentiated Human Umbilical Vein Edothelial Cell Model. PLoS ONE 2012; 7: e38260. doi: 10.1371/journal.pone.0038260 PMID: 22723852
19. Jacobs VR, Niemeyer M, Gottschalk N, Schneider KT, Kiechle M, Oostendorp R, et al. The STEMMATproject as part of health initiative BayernAktiv: adult stem cells from umbilical cord and cord blood as alternative to embryonic stem cell research. Zentralbl Gynakol. 2005; 127: 368-372. PMID: 16341979
20. Wei MC. Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death. Science 2001; 292: 727-730. PMID: 11326099
21. Murphy KM, Ranganathan V, Farnsworth ML, Kavallaris M, Lock RB. Bcl-2 inhibits Bax translocation from cytosol to mitochondria during drug-induced apoptosis of human tumor cells. Cell Death Differ. 2000; 7: 102-111. PMID: 10713725
22. Sosunov SA, Ameer X, Niatsetskaya ZV, Utkina-Sosunova I, Ratner VI, Ten VS. Isoflurane Anesthesia Initiated at the Onset of Reperfusion Attenuates Oxidative and Hypoxic-Ischemic Brain Injury. PLoS ONE 2015; 10: e0120456. doi: 10.1371/journal.pone.0120456 PMID: 25799166
23. Chi OZ, Hunter C, Liu X, Weiss HR. The Effects of Isoflurane Pretreatment on Cerebral Blood Flow, Capillary Permeability, and Oxygen Consumption in Focal Cerebral Ischemia in Rats. Anesth Analg. 2010; 110: 1412-1418. doi: 10.1213/ANE.0b013e3181d6c0ae PMID: 20304986
24. Kuroiwa T, Ting P, Martinez H, Klatzo I. The biphasic opening of the blood-brain barrier to proteins following temporary middle cerebral artery occlusion. Acta Neuropathol. 1985; 68: 122-129. PMID: 3907257
25. Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, et al. The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008; 153: 175-181. doi: 10.1016/j.neuroscience.2008.02.012 PMID: 18367342
26. Pillai DR, Dittmar MS, Baldaranov D, Heidemann RM, Henning EC, Schuierer G, et al. Cerebral ischemia- reperfusion injury in rats - A 3 T MRI study on biphasic blood - brain barrier opening and the dynamics of edema formation. J Cereb Blood Flow Metab. 2009; 29: 1846-1855. doi: 10.1038/jcbfm.2009.106 PMID: 19654585
27. Kuntz M, Mysiorek C, Pétrault O, Pétrault M, Uzbekov R, Bordet R, et al. Stroke-induced brain parenchymal injury drives blood - brain barrier early leakage kinetics: a combined in vivo/in vitro study. J Cereb Blood Flow Metab. 2013; 34: 95-107. doi: 10.1038/jcbfm.2013.169 PMID: 24084699
28. Schwamm LH, Koroshetz WJ, Sorensen AG, Wang B, Copen WA, Budzik R, et al. Time Course of Lesion Development in Patients With Acute Stroke. Serial Diffusion- and Hemodynamic-Weighted Magnetic Resonance Imaging. Stroke 1998; 29: 2268-2276. PMID: 9804633
29. Tétrault S, Chever O, Sik A, Amzica F. Opening of the blood-brain barrier during isoflurane anaesthesia. Eur J Neurosci. 2008; 28: 1330-1341. doi: 10.1111/j.1460-9568.2008.06443.x PMID: 18973560
30. Thal SC, Luh C, Schaible E, Timaru-Kast R, Hedrich J, Luhmann H, et al. Volatile Anesthetics Influence Blood-Brain Barrier Integrity by Modulation of Tight Junction Protein Expression in Traumatic Brain Injury. PLoS ONE 2012; 7: e50752. doi: 10.1371/journal.pone.0050752 PMID: 23251381
31. Liu J, Jin X, Liu KJ, Liu W. Matrix Metalloproteinase-2-Mediated Occludin Degradation and Caveolin-1- Mediated Claudin-5 Redistribution Contribute to Blood-Brain Barrier Damage in Early Ischemic Stroke Stage. J Neurosci. 2012; 32: 3044-3057. doi: 10.1523/JNEUROSCI.6409-11.2012 PMID: 22378877
32. Terrando N, Eriksson LI, Kyu Ryu J, Yang T, Monaco C, Feldmann M, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol. 2011; 70: 986-995. doi: 10.1002/ana.22664 PMID: 22190370
33. He H, Wang Y, Le Y, Duan K, Yan X, Liao Q, et al. Surgery Upregulates High Mobility Group Box-1 and Disrupts the Blood-Brain Barrier causing Cognitive Dysfunction in Aged Rats. CNS Neurosci Ther. 2012; 18: 994-1002. doi: 10.1111/cns.12018 PMID: 23078219
34. Hu N, Guo D, Wang H, Xie K, Wang C, Li Y, et al. Involvement of the blood-brain barrier opening in cognitive decline in aged rats following orthopedic surgery and high concentration of sevoflurane inhalation. Brain Res. 2014; 1551: 13-24. doi: 10.1016/j.brainres.2014.01.015 PMID: 24440777
35. Lee JH, Cui HS, Shin SK, Kim JM, Kim SY, Lee JE, et al. Effect of Propofol Post-treatment on Blood - Brain Barrier Integrity and Cerebral Edema After Transient Cerebral Ischemia in Rats. Neurochem Res. 2013; 38: 2276-2286. doi: 10.1007/s11064-013-1136-7 PMID: 23990224
36. Bezerra FJ, Brown M, Alarcon W, Karki K, Knight RA, Keenan KA, et al. Rate and extent of leakage of a magnetic resonance contrast agent tend to be lower under isoflurane anesthesia in comparison to halothane in a rat model of embolic stroke. Neurol Res. 2014; 36: 847-850. doi: 10.1179/1743132814Y. 0000000341 PMID: 24601723
37. Krueger M, Härtig W, Reichenbach A, Bechmann I, Michalski D. Blood-Brain Barrier Breakdown after Embolic Stroke in Rats Occurs without Ultrastructural Evidence for Disrupting Tight Junctions. PLoS ONE 2013; 8: e56419. doi: 10.1371/journal.pone.0056419 PMID: 23468865
38. Zhang Y, Dong Y, Wu X, Lu Y, Xu Z, Knapp A, et al. The Mitochondrial Pathway of Anesthetic Isoflurane-induced Apoptosis. J Biol Chem. 2010; 285: 4025-4037. doi: 10.1074/jbc.M109.065664 PMID: 20007710
39. Zhang Y, Xu Z, Wang H, Dong Y, Shi HN, Culley DJ, et al. Anesthetics isoflurane and desflurane differently affect mitochondrial function, learning, and memory. Ann Neurol. 2012; 71: 687-698. doi: 10.1002/ana.23536 PMID: 22368036
40. Pétrault M, Ouk T, Lachaud C, Bastide M, Bérézowski V, Pétrault O, et al. Evidence for the Use of Isoflurane as a Replacement for Chloral Hydrate Anesthesia in Experimental Stroke: An Ethical Issue. Biomed Res Int. 2014; 2014: 802539. doi: 10.1155/2014/802539 PMID: 24719888