Characterization and quantification of isoflurane-induced developmental apoptotic cell death in mouse cerebral cortex

Anesthesia and Analgesia

Volumn 116, Issue 4, 2013, Pages 845-854

  Istaphanous, George K ^a,b   Ward, Christopher G ^a,c   Nan, Xinyu ^a   Hughes, Elizabeth A ^a   McCann, John C ^a   McAuliffe, John J ^a   Danzer, Steve C ^a   Loepke, Andreas W ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; ISOFLURANE; PROTEIN S100B;

ANESTHESIA COMPLICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN CORTEX; BRAIN REGION; CELL DENSITY; CELL LOSS; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITE; DIET RESTRICTION; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GABAERGIC SYSTEM; GLIA CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INTERNEURON; LONG TERM EXPOSURE; MALE; MOUSE; NEOCORTEX; NERVE CELL NECROSIS; NONHUMAN; PEDIATRIC ANESTHESIA; PHENOTYPE; PRIORITY JOURNAL; PYRIFORM CORTEX; RETROSPLENIAL CORTEX; VISUAL CORTEX;

ANESTHETICS, INHALATION; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CASPASE 3; CEREBRAL CORTEX; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE; IMMUNOHISTOCHEMISTRY; INTERNEURONS; ISOFLURANE; MALE; MICE; MICE, INBRED C57BL; NEURONS; PHENOTYPE; S100 PROTEINS;

EID: 84876668527     PISSN: 00032999     EISSN: 15267598     Source Type: Journal    
DOI: 10.1213/ANE.0b013e318281e988     Document Type: Article

References (55)

1. DeFrances CJ, Cullen KA, Kozak LJ. National Hospital Discharge Survey: 2005 annual summary with detailed diagnosis and procedure data. Vital Health Stat 2007;13:1-209
2. 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
3. Loepke AW, Istaphanous GK, McAuliffe JJ III, Miles L, Hughes EA, McCann JC, Harlow KE, Kurth CD, Williams MT, Vorhees CV, Danzer SC. The effects of neonatal isoflurane exposure in mice on brain cell viability, adult behavior, learning, and memory. Anesth Analg 2009;108:90-104
4. Stratmann G, May LD, Sall JW, Alvi RS, Bell JS, Ormerod BK, Rau V, Hilton JF, Dai R, Lee MT, Visrodia KH, Ku B, Zusmer EJ, Guggenheim J, Firouzian A. Effect of hypercarbia and isoflurane on brain cell death and neurocognitive dysfunction in 7-day-old rats. Anesthesiology 2009;110:849-61
5. Brambrink AM, Evers AS, Avidan MS, Farber NB, Smith DJ, Zhang X, Dissen GA, Creeley CE, Olney JW. Isofluraneinduced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 2010;112:834-41
6. Rizzi S, Ori C, Jevtovic-Todorovic V. Timing versus duration: determinants of anesthesia-induced developmental apoptosis in the young mammalian brain. Ann NY Acad Sci 2010;1199:43-51
7. 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
8. 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
9. Johnson SA, Young C, Olney JW. Isoflurane-induced neuroapoptosis in the developing brain of nonhypoglycemic mice. J Neurosurg Anesthesiol 2008;20:21-8
10. Henschel O, Gipson KE, Bordey A. GABAA receptors, anesthetics and anticonvulsants in brain development. CNS Neurol Disord Drug Targets 2008;7:211-24
11. Paxinos G, Franklin KB. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. San Diego: Academic Press, 2001
12. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;231:482-97
13. West MJ. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 1999;22:51-61
14. Graham PL, Mengersen K, Morton AP. Confidence limits for the ratio of two rates based on likelihood scores: non-iterative method. Stat Med 2003;22:2071-83
15. Rothman KJ, Greenland S. Modern Epidemiology. 2nd ed. Philadelphia: Lippincott-Raven, 1998
16. Wei H, Kang B, Wei W, Liang G, Meng QC, Li Y, Eckenhoff RG. Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Res 2005;1037:139-47
17. Wise-Faberowski L, Zhang H, Ing R, Pearlstein RD, Warner DS. Isoflurane-induced neuronal degeneration: an evaluation in organotypic hippocampal slice cultures. Anesth Analg 2005;101:651-7
18. Wei H, Liang G, Yang H. Isoflurane preconditioning inhibited isoflurane-induced neurotoxicity. Neurosci Lett 2007;425:59-62
19. 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
20. 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
21. Stratmann G, Sall JW, May LD, Bell JS, Magnusson KR, Rau V, Visrodia KH, Alvi RS, Ku B, Lee MT, Dai R. Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats. Anesthesiology 2009;110:834-48
22. Jevtovic-Todorovic V, Olney JW. PRO: anesthesia-induced developmental neuroapoptosis-status of the evidence. Anesth Analg 2008;106:1659-63
23. Loepke AW, McGowan FX Jr, Soriano SG. CON: the toxic effects of anesthetics in the developing brain: the clinical perspective. Anesth Analg 2008;106:1664-9
24. Loepke AW. Developmental neurotoxicity of sedatives and anesthetics: a concern for neonatal and pediatric critical care medicine? Pediatr Crit Care Med 2010;11:217-26
25. Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992;116:201-11
26. Lyck L, Krøigård T, Finsen B. Unbiased cell quantification reveals a continued increase in the number of neocortical neurones during early post-natal development in mice. Eur J Neurosci 2007;26:1749-64
27. 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
28. Sall JW, Stratmann G, Leong J, McKleroy W, Mason D, Shenoy S, Pleasure SJ, Bickler PE. Isoflurane inhibits growth but does not cause cell death in hippocampal neural precursor cells grown in culture. Anesthesiology 2009;110:826-33
29. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 1972;145:61-83
30. Aschner M, Sonnewald U, Tan KH. Astrocyte modulation of neurotoxic injury. Brain Pathol 2002;12:475-81
31. Stevens B. Neuron-astrocyte signaling in the development and plasticity of neural circuits. Neurosignals 2008;16:278-88
32. Anderson MF, Blomstrand F, Blomstrand C, Eriksson PS, Nilsson M. Astrocytes and stroke: networking for survival? Neurochem Res 2003;28:293-305
33. Yu AC, Wong HK, Yung HW, Lau LT. Ischemia-induced apoptosis in primary cultures of astrocytes. Glia 2001;35:121-30
34. Yang Q, Hamberger A, Khatibi N, Stigbrand T, Haglid KG. Presence of S-100 beta in cholinergic neurones of the rat hindbrain. Neuroreport 1996;7:3093-9
35. Vives V, Alonso G, Solal AC, Joubert D, Legraverend C. Visualization of S100B-positive neurons and glia in the central nervous system of EGFP transgenic mice. J Comp Neurol 2003;457:404-19
36. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 1991;14:453-501
37. Rakic S, Zecevic N. Programmed cell death in the developing human telencephalon. Eur J Neurosci 2000;12:2721-34
38. Hodge RD, D'Ercole AJ, O'Kusky JR. Insulin-like growth factor-I (IGF-I) inhibits neuronal apoptosis in the developing cerebral cortex in vivo. Int J Dev Neurosci 2007;25:233-41
39. Fagel DM, Ganat Y, Silbereis J, Ebbitt T, Stewart W, Zhang H, Ment LR, Vaccarino FM. Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp Neurol 2006;199:77-91
40. Buddhala C, Hsu CC, Wu JY. A novel mechanism for GABA synthesis and packaging into synaptic vesicles. Neurochem Int 2009;55:9-12
41. Kanaani J, Kolibachuk J, Martinez H, Baekkeskov S. Two distinct mechanisms target GAD67 to vesicular pathways and presynaptic clusters. J Cell Biol 2010;190:911-25
42. Erlander MG, Tobin AJ. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem Res 1991;16:215-26
43. Zhou ZW, Shu Y, Li M, Guo X, Pac-Soo C, Maze M, Ma D. The glutaminergic, GABAergic, dopaminergic but not cholinergic neurons are susceptible to anaesthesia-induced cell death in the rat developing brain. Neuroscience 2011;174:64-70
44. Honegger P, Pardo B, Monnet-Tschudi F. Muscimol-induced death of GABAergic neurons in rat brain aggregating cell cultures. Brain Res Dev Brain Res 1998;105:219-25
45. Honegger P, Matthieu JM. Selective toxicity of the general anesthetic propofol for GABAergic neurons in rat brain cell cultures. J Neurosci Res 1996;45:631-6
46. Baptista MS, Melo CV, Armelão M, Herrmann D, Pimentel DO, Leal G, Caldeira MV, Bahr BA, Bengtson M, Almeida RD, Duarte CB. Role of the proteasome in excitotoxicity-induced cleavage of glutamic acid decarboxylase in cultured hippocampal neurons. PLoS One 2010;5:e10139
47. Beaulieu C. Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 1993;609:284-92
48. Lee M, Schwab C, McGeer PL. Astrocytes are GABAergic cells that modulate microglial activity. Glia 2011;59:152-65
49. Wilder RT, Flick RP, Sprung J, Katusic SK, Barbaresi WJ, Mickelson C, Gleich SJ, Schroeder DR, Weaver AL, Warner DO. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 2009;110:796-804
50. DiMaggio C, Sun LS, Li G. Early childhood exposure to anesthesia and risk of developmental and behavioral disorders in a sibling birth cohort. Anesth Analg 2011;113:1143-51
51. Rozé JC, Denizot S, Carbajal R, Ancel PY, Kaminski M, Arnaud C, Truffert P, Marret S, Matis J, Thiriez G, Cambonie G, André M, Larroque B, Bréart G. Prolonged sedation and/or analgesia and 5-year neurodevelopment outcome in very preterm infants: results from the EPIPAGE cohort. Arch Pediatr Adolesc Med 2008;162:728-33
52. Bartels M, Althoff RR, Boomsma DI. Anesthesia and cognitive performance in children: no evidence for a causal relationship. Twin Res Hum Genet 2009;12:246-53
53. Guerra GG, Robertson CM, Alton GY, Joffe AR, Cave DA, Dinu IA, Creighton DE, Ross DB, Rebeyka IM; Western Canadian Complex Pediatric Therapies Follow-up Group. Neurodevelopmental outcome following exposure to sedative and analgesic drugs for complex cardiac surgery in infancy. Paediatr Anaesth 2011;21:932-41
54. Dobbing J, Sands J. Quantitative growth and development of human brain. Arch Dis Child 1973;48:757-67
55. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience 2001;105:7-17