Early exposure to general anesthesia disturbs mitochondrial fission and fusion in the developing rat brain

Anesthesiology

Volumn 118, Issue 5, 2013, Pages 1086-1097

  Boscolo, Annalisa ^a,b   Milanovic, Desanka ^a,c   Starr, John A ^a   Sanchez, Victoria ^a   Oklopcic, Azra ^a   Moy, Laurie ^a   Ori C, Carlo ^b   Erisir, Alev ^a   Jevtovic Todorovic, Vesna ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; ISOFLURANE; MIDAZOLAM; NITROUS OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL FRACTIONATION; CELL FUSION; CELL REGENERATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; GENERAL ANESTHESIA; HISTOPATHOLOGY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MORPHOGENESIS; MORPHOMETRICS; NERVE CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; RAT; SYNAPTOGENESIS; UPREGULATION;

ANESTHESIA, GENERAL; ANIMALS; BLOTTING, WESTERN; BRAIN; CATALASE; CYTOPLASM; DOWN-REGULATION; DYNAMINS; HOMEOSTASIS; MEMBRANE PROTEINS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE;

EID: 84877583431     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e318289bc9b     Document Type: Article

References (40)

1. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF: Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003; 23:876-82
2. Rizzi S, Carter LB, Ori C, Jevtovic-Todorovic V: Clinical anesthesia causes permanent damage to the fetal guinea pig brain. Brain Pathol 2008; 18:198-210
3. Slikker W Jr, Zou X, Hotchkiss CE, Divine RL, Sadovova N, Twaddle NC, Doerge DR, Scallet AC, Patterson TA, Hanig JP, Paule MG, Wang C: Ketamine-induced neuronal cell death in the perinatal rhesus monkey. Toxicol Sci 2007; 98:145-58
4. Yon JH, 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; 135:815-27
5. 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
6. Lunardi N, Ori C, Erisir A, Jevtovic-Todorovic V: General anesthesia causes long-lasting disturbances in the ultrastructural properties of developing synapses in young rats. Neurotox Res 2010; 17:179-88
7. Briner A, De Roo M, Dayer A, Muller D, Habre W, Vutskits L: Volatile anesthetics rapidly increase dendritic spine density in the rat medial prefrontal cortex during synaptogenesis. Anesthesiology 2010; 112:546-56
8. Briner A, Nikonenko I, De Roo M, Dayer A, Muller D, Vutskits L: Developmental stage-dependent persistent impact of propofol anesthesia on dendritic spines in the rat medial prefrontal cortex. Anesthesiology 2011; 115:282-93
9. 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
10. Sanchez V, Feinstein SD, Lunardi N, Joksovic PM, Boscolo A, Todorovic SM, Jevtovic-Todorovic V: General anesthesia causes long-term impairment of mitochondrial morphogenesis and synaptic transmission in developing rat brain. Anesthesiology 2011; 115:992-1002
11. Chan DC: Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 2006; 22:79-99
12. Yoon Y, Pitts KR, McNiven MA: Mammalian dynamin-like protein DLP1 tubulates membranes. Mol Biol Cell 2001; 12:2894-905
13. Smirnova E, Griparic L, Shurland DL, van der Bliek AM: Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 2001; 12:2245-56
14. Koshiba T, Detmer SA, Kaiser JT, Chen H, McCaffery JM, Chan DC: Structural basis of mitochondrial tethering by mitofusin complexes. Science 2004; 305:858-62
15. Chen H, Chomyn A, Chan DC: Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 2005; 280:26185-92
16. Boscolo A, Starr JA, Sanchez V, Lunardi N, DiGruccio MR, Ori C, Erisir A, Trimmer P, Bennett J, Jevtovic-Todorovic V: The abolishment of anesthesia-induced cognitive impairment by timely protection of mitochondria in the developing rat brain: The importance of free oxygen radicals and mitochondrial integrity. Neurobiol Dis 2012; 45:1031-41
17. Jevtovic-Todorovic V, Benshoff N, Olney JW: Ketamine potentiates cerebrocortical damage induced by the common anaesthetic agent nitrous oxide in adult rats. Br J Pharmacol 2000; 130:1692-8
18. Lu LX, Yon JH, Carter LB, Jevtovic-Todorovic V: General anesthesia activates BDNF-dependent neuroapoptosis in the developing rat brain. Apoptosis 2006; 11:1603-15
19. Yon JH, Carter LB, Reiter RJ, Jevtovic-Todorovic V: Melatonin reduces the severity of anesthesia-induced apoptotic neurodegeneration in the developing rat brain. Neurobiol Dis 2006; 21:522-30
20. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. Australia, Academic Press, 1944
21. Tian C, Murrin LC, Zheng JC: Mitochondrial fragmentation is involved in methamphetamine-induced cell death in rat hippocampal neural progenitor cells. PLoS ONE 2009; 4: e5546
22. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL, Youle RJ: The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001; 1:515-25
23. Youle RJ, Karbowski M: Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 2005; 6:657-63
24. Barsoum MJ, Yuan H, Gerencser AA, Liot G, Kushnareva Y, Gräber S, Kovacs I, Lee WD, Waggoner J, Cui J, White AD, Bossy B, Martinou JC, Youle RJ, Lipton SA, Ellisman MH, Perkins GA, Bossy-Wetzel E: Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J 2006; 25:3900-11
25. Crichton RR, Ward RJ: Oxidative Stress and Redox Active Metal Ions. Crichton RR, Ward RJ (eds.), Metal-based Neurodegeneration: From Molecular Mechanisms to Therapeutic Strategies. John Wiley & Sons, 2006; Chapter 2, pp 21-51
26. Costantini P, Belzacq AS, Vieira HL, Larochette N, de Pablo MA, Zamzami N, Susin SA, Brenner C, Kroemer G: Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 2000; 19:307-14
27. Reddy PH, Reddy TP, Manczak M, Calkins MJ, Shirendeb U, Mao P: Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases. Brain Res Rev 2011; 67:103-18
28. Grohm J, Kim SW, Mamrak U, Tobaben S, Cassidy-Stone A, Nunnari J, Plesnila N, Culmsee C: Inhibition of Drp1 provides neuroprotection in vitro and in vivo. Cell Death Differ 2012; 19:1446-58
29. Breckenridge DG, Stojanovic M, Marcellus RC, Shore GC: Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol 2003; 160:1115-27
30. Germain M, Mathai JP, McBride HM, Shore GC: Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J 2005; 24:1546-56
31. Wu S, Zhou F, Zhang Z, Xing D: Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS J 2011; 278:941-54
32. Sheridan C, Delivani P, Cullen SP, Martin SJ: Bax-or Bakinduced mitochondrial fission can be uncoupled from cytochrome C release. Mol Cell 2008; 31:570-85
33. Scorrano L: Opening the doors to cytochrome c: Changes in mitochondrial shape and apoptosis. Int J Biochem Cell Biol 2009; 41:1875-83
34. Abramov AY, Scorziello A, Duchen MR: Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 2007; 27:1129-38
35. Bach D, Pich S, Soriano FX, Vega N, Baumgartner B, Oriola J, Daugaard JR, Lloberas J, Camps M, Zierath JR, Rabasa-Lhoret R, Wallberg-Henriksson H, Laville M, Palacín M, Vidal H, Rivera F, Brand M, Zorzano A: Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J Biol Chem 2003; 278:17190-7
36. Pich S, Bach D, Briones P, Liesa M, Camps M, Testar X, Palacín M, Zorzano A: The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet 2005; 14:1405-15
37. Delivani P, Adrain C, Taylor RC, Duriez PJ, Martin SJ: Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol Cell 2006; 21:761-73
38. Jahani-Asl A, Cheung EC, Neuspiel M, MacLaurin JG, Fortin A, Park DS, McBride HM, Slack RS: Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J Biol Chem 2007; 282:23788-98
39. Yu T, Robotham JL, Yoon Y: Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA 2006; 103:2653-8
40. Li J, Liu X, Wang H, Zhang W, Chan DC, Shi Y: Lysocardiolipin acyltransferase 1 (ALCAT1) controls mitochondrial DNA fidelity and biogenesis through modulation of MFN2 expression. Proc Natl Acad Sci USA 2012; 109:6975-80