Effects of vitamin C on inhalation anesthetic isoflurane-induced developmental, neuronal apoptosis in neonatal rats
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https://doi.org/10.3329/bjp.v9i4.20534Keywords:
Vitamin C, isoflurane, neuronal apoptosis, neurotoxicityAbstract
Developmental abnormalities, neuronal apoptosis and associated cognitive impairment following isoflurane exposure in neonatal rodents have been reported. The study was undertaken to investigate the effect of vitamin C supplementation against isoflurane-induced neurotoxicity. Seven day old rats were exposed to 1.1% isoflurane, or air for 6 hours. Treatment groups were administered with vitamin C (30 mg/kg, orally) from postnatal day 1 (P1) to P10 and were exposed to isoflurane on P7. Isoflurane exposure induced apoptosis was determined by Fluoro-Jade C and terminal deoxynucleotidyl-transferase-mediated 2-deoxyuridine 5-triphosphate nick-end labeling assay. Vitamin C considerably improved memory and learning impairments, modulated neuroapoptosis and improved expressions of brain-derived neurotrophic factor, nerve growth factor, Bcl-xL and decreased activated caspase-3 expressions. Thus, vitamin C effectively offered protection against isoflurane-induced neuronal apoptosis, learning and memory disturbances.
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Almeida RD, Manadas BJ, Melo CV, Gomes JR, Mendes CS, Graos MM, Carvalho RF, Carvalho AP, Duarte CB. Neuroprotection by BDNF against glutamate induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 2005; 12: 1329-43.
Bath KG, Schilit A, Lee FS. Stress effects on BDNF expression: Effects of age, sex, and form of stress. Neuroscience 2013; 239: 149-56.
Bianchi P, Ciani E, Guidi S, Trazzi S, Felice D, Grossi G, Fernandez M, Giuliani A, Calza L, Bartesaghi R. Early pharmacotherapy restores neurogenesis and cognitive per-formance in the Ts65Dn mouse model for Down syndrome. J Neurosci. 2010; 30: 8769-79.
Bibel M, Barde YA. Neurotrophins: Key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev. 2000; 14: 2919-37.
Brambrink AM, Evers AS, Avidan MS, Farber NB, Smith DJ, Zhang X, Dissen GA, Creeley CE, Olney JW. Isoflurane-induced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 2010; 112: 834-41.
Brambrink AM, Back SA, Riddle A, Gong X, Moravec MD, Dissen GA, Creeley CE, Dikranian KT, Olney JW. Isoflurane-induced apoptosis of oligodendrocytes in the neonatal primate brain. Ann Neurol. 2012; 72: 525-35.
Chu R, Upreti M, Ding WX, Yin XM, Chambers TC. Regulation of Bax by c-Jun NH2-terminal kinase and Bcl-xL in vinblastine-induced apoptosis. Biochem Pharmacol. 2009; 78: 241-48.
Denis-Donini S, Dellarole A, Crociara P, Francese MT, Bortolotto V, Quadrato G, Canonico PL, Orsetti M, Ghi P, Memo M, Bonini SA, Ferrari-Toninelli G, Grilli M. Impaired adult neurogenesis associated with short-term memory defects in NF-kappaB p50-deficient mice. J Neurosci. 2008; 28: 3911-19.
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.
Dong Y, Zhang G, Zhang B, Moir RD, Xia W, Marcantonio ER, Culley DJ, Crosby G, Tanzi RE, Xie Z. The common inhalational anesthetic sevoflurane induces apoptosis and increases beta-amyloid protein levels. Arch Neurol. 2009; 66: 620-31.
Husson I, Rangon CM, Lelievre V, Bemelmans AP, Sachs P, Mallet J, Kosofsky BE, Gressens P. BDNF-induced white matter neuroprotection and stage-dependent neuronal survival following a neonatal excitotoxic challenge. Cereb Cortex. 2005; 15: 250-61.
Ing C, DiMaggio C, Whitehouse A, Hegarty MK, Brady J, von Ungern-Sternberg BS, Davidson A, Wood AJ, Li G, Sun LS. Long-term differences in lan-guage and cognitive function after childhood exposure to anesthesia. Pediatrics 2012; 130: e476-85.
Istaphanous GK, Loepke AW. General anesthetics and the developing brain. Curr Opin Anesthesiol. 2009; 22: 368-73.
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.
Jeong HS, Choi HY, Choi TW, Kim BW, Kim JH, Lee ER, Cho SG. Differential regulation of the antiapoptotic action of B-cell lymphoma 2 (Bcl-2) and B-cell lymphoma extra long (Bcl-xL) by c-Jun N-terminal protein kinase (JNK) 1-involved pathway in neuroglioma cells. Biol Pharm Bull. 2008; 31: 1686-90.
Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorum-ski 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.
Kong F, Xu L, He D, Zhang X, Lu H. Effects of gestational isoflurane exposure on postnatal memory and learning in rats. Eur J Pharmacol. 2011; 670: 168-74.
Kovacic P, Somanathan R. Unifying mechanism for eye toxicity: Electron transfer, reactive oxygen species, antioxidant benefits, cell signaling and cell membranes. Cell Membr Free Radic Res. 2008; 2: 56-69.
Li Y, Liang G, Wang S, Meng Q, Wang Q, Wei H. Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology 2007; 53: 942-50.
Li C, Xing G, Dong M, Zhou L, Li J, Wang G, Zou D, Wang R, Liu J, Niu Y. Beta asarone protection against beta-amyloid-induced neurotoxicity in PC12 cells via JNK signaling and modulation of Bcl-2 family proteins. Eur J Pharmacol. 2010; 635: 96-102.
Li Y, Liu C, Zhao Y, Hu K, Zhang J, Zeng M, Luo T, Jiang W, Wang H. Sevoflurane induces short-term changes in proteins in the cerebral cortices of developing rats. Acta Anaesthesiol Scand. 2013a; 57: 380-90.
Li Y, Wang F, Liu C, Zeng M, Han X, Luo T, Jiang W, Xu J, Wang H. JNK pathway may be involved in isoflurane-induced apoptosis in the hippocampi of neonatal rats. Neurosci Lett. 2013b; 545: 17-22.
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.
Ma D, Williamson P, Januszewski A, Nogaro MC, Hossain M, Ong LP, Shu Y, Franks NP, Maze M. Xenon mitigates isoflurane-induced neuronal apoptosis in the developing rodent brain. Anesthesiology 2007; 106: 746-53.
Moonesinghe SR, Mythen MG, Grocott MP. High-risk surgery: epidemiology and outcomes. Anesth Analg. 2011; 112: 891?901.
Nazirolu M, Cay M. Protective role of intraperitoneally administered vitamin E and selenium on the antioxidative defense mechanisms in rats with diabetes induced by streptozotocin. Biol Trace Elem Res. 2001; 79: 149-59.
Nazirolu M, Gunay C. The levels of some antioxidant vitamins, glutathione peroxidase and lipoperoxidase during the anaesthesia of dogs. Cell Biochem Funct. 1999; 17: 207-12.
Netke SP, Roomi MW, Tsao C, Niedzwiecki A. Ascorbic acid protects guinea pigs from acute aflatoxin toxicity. Toxicol Appl Pharmacol. 1997; 143: 429-35.
Nguyen TL, Kim CK, Cho JH, Lee KH, Ahn JY. Neuroprotec-tion signaling pathway of nerve growth factor and brain-derived neurotrophic factor against staurosporine induced apoptosis in hippocampal H19-7/IGF-IR. Exp Mol Med. 2010; 42: 583-95.
Orliaguet G, Vivien B, Langeron O, Bouhemad B, Coriat P, Riou B. Minimum alveolar concentration of volatile anesthe-tics in rats during postnatal maturation. Anesthesiology 2001; 95: 34-39.
Paule MG, Li M, Allen RR, Liu F, Zou X, Hotchkiss C, Hanig JP, Patterson TA, Slikker WJ, Wang C. Ketamine anesthesia during the first week of life can cause long-lasting cognitive deficits in rhesus monkeys. Neurotoxicol Teratol. 2011; 33: 220-30.
Rice D, Barone Jr. S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 2000; 108(Suppl. 3): 511-33.
Sanders RD, Xu J, Shu Y, Januszewski A, Halder S, Fidalgo A, Sun P, Hossain M, Ma D, Maze M. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats. Anesthesiology 2009; 110: 1077-85.
Sanders RD, Sun P, Patel S, Li M, Maze M, Ma D. Dexmedetomidine provides cortical neuroprotection: impact on anaesthetic-induced neuroapoptosis in the rat developing brain. Acta Anaesthesiol Scand. 2010; 54: 710-16.
Satomoto M, Satoh Y, Terui K, Miyao H, Takishima K, Ito M, Imaki J. Neonatal exposure to sevoflurane induces abnormal social behaviors and deficitsin fear conditioning in mice. Anesthesiology 2009; 110: 628-37.
Shih J, May LD, Gonzalez HE, Lee EW, Alvi RS, Sall JW, Rau V, Bickler PE, Lalchandani GR, Yusupova M, Woodward E, Kang H, Wilk AJ, Carlston CM, Mendoza MV, Guggenheim JN, Schaefer M, Rowe AM, Stratmann G. Delayed environmental enrichment reverses sevoflurane induced memory impairment in rats. Anesthesiology 2012; 116: e586-e602.
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 2009b; 110: e834-48.
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.
Weiser TG, Regenbogen SE, Thompson KD, Haynes AB, Lipsitz SR, Berry WR, Gawande AA. An estimation of the global volume of surgery: a modelling strategy based on available data. Lancet. 2008; 372: 139?44.
Xie ZC, Dong YL, Maeda U, Moir RD, Xia WM, Culley DJ, Crosby G, Tanzi RE. The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid beta-protein accumulation. J Neurosci. 2007; 27: 1247-54.
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.
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.
Zhao H, Yenari MA, Cheng D, Sapolsky RM, Steinberg GK. Bcl-2 overexpression protects against neuron loss within the ischemic margin following experimental stroke and inhibits cytochrome c translocation and caspase-3 activity. J Neurochem. 2003; 85: 1026-36.
Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008; 132: 645-60.
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