Time-Dependent effects of anesthetic isoflurane on reactive oxygen species levels in HEK-293 cells

Brain Sciences

Volumn 4, Issue 2, 2014, Pages 311-320

  Sun, Yongxing ^a,b   Cheng, Baiqi ^a   Dong, Yuanlin ^a   Li, Tianzuo ^b   Xie, Zhongcong ^a   Zhang, Yiying ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Isoflurane; Mitochondria; Reactive oxygen species

Indexed keywords

CASPASE; CYTOCHROME C; ISOFLURANE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENZYME ACTIVITY; FLUORESCENCE IMAGING; HEK293 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; LEARNING DISORDER; MEMORY DISORDER; MITOCHONDRIAL MEMBRANE POTENTIAL; PILOT STUDY; QUANTITATIVE ASSAY;

EID: 84918541651     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci4020311     Document Type: Article

References (38)

1. Wilder, R.T.; Flick, R.P.; Sprung, J.; Katusic, S.K.; Barbaresi, W.J.; Mickelson, C.; Gleich, S.J.; Schroeder, D.R.; Weaver, A.L.; Warner, D.O. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 2009, 110, 796-804.
2. Flick, R.P.; Katusic, S.K.; Colligan, R.C.; Wilder, R.T.; Voigt, R.G.; Olson, M.D.; Sprung, J.; Weaver, A.L.; Schroeder, D.R.; Warner, D.O. Cognitive and behavioral outcomes after early exposure to anesthesia and surgery. Pediatrics 2011, 128, e1053-e1061.
3. Sun, L. Early childhood general anaesthesia exposure and neurocognitive development. Br. J. Anaesth 2010, 105, i61-i68.
4. Jevtovic-Todorovic, V.; Hartman, R.E.; Izumi, Y; Benshoff, N.D.; Dikranian, K.; Zorumski, C.F.; Olney, J.W.; Wozniak, D.F. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J. Neurosci. 2003, 23, 876-882.
5. Satomoto, M.; Satoh, Y.; Terui, K.; Miyao, H.; Takishima, K.; Ito, M.; Imaki, J. Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 2009, 110, 628-637.
6. Stratmann, G.; Sall, J.W.; May, L.D.; Bell, J.S.; Magnusson, K.R.; Rau, V.; Visrodia, K.H.; Alvi, R.S.; Ku, B.; Lee, M.T. et al. Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats. Anesthesiology 2009, 110, 834-848.
7. Brambrink, A.M.; Back, S.A.; Riddle, A.; Gong, X.; Moravec, M.D.; Dissen, G.A.; Creeley, C.E.; Dikranian, K.T.; Olney, J.W. Isoflurane-induced apoptosis of oligodendrocytes in the neonatal primate brain. Ann. Neurol. 2012, 72, 525-535.
8. Brambrink, A.M.; Evers, A.S.; Avidan, M.S.; Farber, N.B.; Smith, D.J.; Zhang, X.; Dissen, G.A.; Creeley, C.E.; Olney, J.W. Isoflurane-induced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 2010, 112, 834-841.
9. Eckenhoff, R.G.; Johansson, J.S.; Wei, H.; Carnini, A.; Kang, B.; Wei, W.; Pidikiti, R.; Keller, J.M.; Eckenhoff, M.F. Inhaled anesthetic enhancement of amyloid-beta oligomerization and cytotoxicity. Anesthesiology 2004, 101, 703-709.
10. Xie, Z.; Dong, Y.; Maeda, U; Moir, R.D.; Xia, W.; Culley, D.J.; Crosby, G.; Tanzi, R.E. The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid beta-protein accumulation. J. Neurosci. 2007, 27, 1247-1254.
11. Xie, Z.; Dong, Y.; Maeda, U.; Moir, R.; Inouye, S.K.; Culley, D.J.; Crosby, G.; Tanzi, R.E. Isoflurane-induced apoptosis: A potential pathogenic link between delirium and dementia. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61, 1300-1306.
12. Xie, Z.; Dong, Y.; Maeda, U.; Alfille, P.; Culley, D.J.; Crosby, G.; Tanzi, R.E. The common inhalation anesthetic isoflurane induces apoptosis and increases amyloid beta protein levels. Anesthesiology 2006, 104, 988-994.
13. Xie, Z.; Culley, D.J.; Dong, Y.; Zhang, G.; Zhang, B.; Moir, R.D.; Frosch, M.P.; Crosby, G.; Tanzi, R.E. The common inhalation anesthetic isoflurane induces caspase activation and increases amyloid beta-protein level in vivo. Ann. Neurol. 2008, 64, 618-627.
14. Wei, H.; Liang, G.; Yang, H. Isoflurane preconditioning inhibited isoflurane-induced neurotoxicity. Neurosci. Lett. 2007, 425, 59-62.
15. Wei, H.; Kang, B.; Wei, W.; Liang, G.; Meng, Q.C.; Li, Y.; Eckenhoff, R.G. Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Res. 2005, 1037, 139-147.
16. Shu, Y.; Zhou, Z.; Wan, Y.; Sanders, R.D.; Li, M.; Pac-Soo, C.K.; Maze, M.; Ma, D. Nociceptive stimuli enhance anesthetic-induced neuroapoptosis in the rat developing brain. Neurobiol. Dis. 2012, 45, 743-750.
17. Good, P.F.; Werner, P.; Hsu, A.; Olanow, C.W.; Perl, D.P. Evidence of neuronal oxidative damage in Alzheimer's disease. Am. J. Pathol. 1996, 149, 21-28.
18. Smith, M.A.; Perry, G.; Richey, P.L.; Sayre, L.M.; Anderson, V.E.; Beal, M.F.; Kowall, N. Oxidative damage in Alzheimer's. Nature 1996, 382, 120-121.
19. Querfurth, H.W.; LaFerla, F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362, 329-344.
20. Markesbery, W.R. The role of oxidative stress in Alzheimer disease. Arch. Neurol. 1999, 56, 1449-1452.
21. Simon, H.U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415-418.
22. Chen, Q.; Vazquez, E.J.; Moghaddas, S.; Hoppel, C.L.; Lesnefsky, E.J. Production of reactive oxygen species by mitochondria: Central role of complex III. J. Biol. Chem. 2003, 278, 36027-36031.
23. Hirata, N.; Shim, Y.H.; Pravdic, D.; Lohr, N.L.; Pratt, P.F., Jr.; Weihrauch, D.; Kersten, J.R.; Warltier, D.C.; Bosnjak, Z.J.; Bienengraeber, M. Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward vs. reverse electron transport flow: Implications for preconditioning. Anesthesiology 2011, 115, 531-540.
24. Kayser, E.B.; Suthammarak, W.; Morgan, P.G.; Sedensky, M.M. Isoflurane selectively inhibits distal mitochondrial complex I in Caenorhabditis elegans. Anesth. Analg. 2011, 112, 1321-1329.
25. Zhang, Y.; Xu, Z.; Wang, H.; Dong, Y.; Shi, H.N.; Culley, D.J.; Crosby, G.; Marcantonio, E.R.; Tanzi, R.E.; Xie, Z. Anesthetics isoflurane and desflurane differently affect mitochondrial function, learning, and memory. Ann. Neurol. 2012, 71, 687-698.
26. Zhang, Y.; Dong, Y.; Wu, X.; Lu, Y.; Xu, Z.; Knapp, A.; Yue, Y.; Xu, T.; Xie, Z. The mitochondrial pathway of anesthetic isoflurane-induced apoptosis. J. Biol. Chem. 2010, 285, 4025-4037.
27. Sancak, Y.; Markhard, A.L.; Kitami, T.; Kovacs-Bogdan, E.; Kamer, K.J.; Udeshi, N.D.; Carr, S.A; Chaudhuri, D.; Clapham, D.E.; Li, A.A. et al. EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 2013, 342, 1379-1382.
28. Dong, Y.; Zhang, G.; Zhang, B.; Moir, R.D.; Xia, W.; Marcantonio, E.R.; Culley, D.J.; Crosby, G.; Tanzi, R.E.; Xie, Z. The common inhalational anesthetic sevoflurane induces apoptosis and increases beta-amyloid protein levels. Arch. Neurol 2009, 66, 620-631.
29. Zhang, G.; Dong, Y.; Zhang, B.; Ichinose, F.; Wu, X.; Culley, D.J.; Crosby, G.; Tanzi, R.E.; Xie, Z. Isoflurane-induced caspase-3 activation is dependent on cytosolic calcium and can be attenuated by memantine. J. Neurosci. 2008, 28, 4551-4560.
30. Zhang, B.; Tian, M.; Zhen, Y.; Yue, Y.; Sherman, J.; Zheng, H.; Li, S.; Tanzi, R.E.; Marcantonio, E.R.; Xie, Z. The effects of isoflurane and desflurane on cognitive function in humans. Anesth. Analg. 2012, 114, 410-415.
31. Droge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82, 47-95.
32. Gupta, S.; Agarwal, A.; Krajcir, N.; Alvarez, J.G. Role of oxidative stress in endometriosis. Reprod. Biomed. Online 2006, 13, 126-134.
33. Yang, Q.; Dong, H.; Deng, J.; Wang, Q.; Ye, R.; Li, X.; Hu, S.; Dong, H.; Xiong, L. Sevoflurane preconditioning induces neuroprotection through reactive oxygen species-mediated up-regulation of antioxidant enzymes in rats. Anesth. Analg. 2011, 112, 931-937.
34. Ohtsuki, T.; Matsumoto, M.; Kuwabara, K.; Kitagawa, K.; Suzuki, K.; Taniguchi, N.; Kamada, T. Influence of oxidative stress on induced tolerance to ischemia in gerbil hippocampal neurons. Brain Res. 1992, 599, 246-252.
35. Sedlic, F.; Pravdic, D.; Ljubkovic, M.; Marinovic, J.; Stadnicka, A.; Bosnjak, Z.J. Differences in production of reactive oxygen species and mitochondrial uncoupling as events in the preconditioning signaling cascade between desflurane and sevoflurane. Anesth. Analg. 2009, 109, 405-411.
36. Lamberts, R.R.; Onderwater, G.; Hamdani, N.; Vreden, M.J.; Steenhuisen, J.; Eringa, E.C.; Loer, S.A.; Stienen, G.J.; Bouwman, R.A. Reactive oxygen species-induced stimulation of 5′AMP-activated protein kinase mediates sevoflurane-induced cardioprotection. Circulation 2009, 120, S10-S15.
37. Venditti, P.; di Stefano, L.; di Meo, S. Mitochondrial metabolism of reactive oxygen species. Mitochondrion 2013, 13, 71-82.
38. 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, 741-752.