Skip to main content
Top
Published in: BMC Anesthesiology 1/2017

Open Access 01-12-2017 | Research article

Hydrogen sulfide attenuates isoflurane-induced neuroapoptosis and cognitive impairment in the developing rat brain

Authors: Xueyuan Hu, Li Luan, Wei Guan, Shuai Zhang, Bei Li, Wei Ji, Honggang Fan

Published in: BMC Anesthesiology | Issue 1/2017

Login to get access

Abstract

Background

Isoflurane-induced neuroapoptosis and cognitive impairment has been previously reported. Hydrogen sulfide (H2S) has been shown to be a neuromodulator that is thought to have anti-apoptotic, anti-inflammatory, and anti-oxidative benefits. However, it is not known if H2S is protective against anesthesia-induced apoptosis and cognitive defects.

Methods

In this study, postnatal day 7 (P7) Sprague-Dawley rats were randomly divided into four groups: control group (normal saline), H2S group (NaHS 28 μM/kg), isoflurane group (normal saline +0.75% isoflurane) and H2S preconditioning group (NaHS 28 μM/kg + 0.75% isoflurane). After exposure to isoflurane for 6 h, half the numbers of rats in each group were euthanized, and the hippocampus and cerebral cortex were dissected and examined for apoptosis by the terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling (TUNEL) technique and western blot. After 6 weeks, the remaining rats were subjected to a Morris water maze (MWM) test for behavioral assessment.

Results

The TUNEL assay and western blot showed that when rats were preconditioned with NaHS, neuroapoptosis decreased significantly both in hippocampus and cerebral cortex compering with the isofulrane group. The MWM showed that P7 rats administration of NaHS improved cognitive impairments induced by isoflurane.

Conclusions

The current study demonstrates that H2S attenuates isoflurane-induced neuroapoptosis and improves cognitive impairments in the developing rat brain.
Literature
1.
go back to reference Sakai H, Sheng H, Yates RB, Ishida K, Pearlstein RD, Warner DS. Isoflurane provides long-term protection against focal cerebral ischemia in the rat. Anesthesiology. 2007;106(1):92–9. discussion 98-10CrossRefPubMed Sakai H, Sheng H, Yates RB, Ishida K, Pearlstein RD, Warner DS. Isoflurane provides long-term protection against focal cerebral ischemia in the rat. Anesthesiology. 2007;106(1):92–9. discussion 98-10CrossRefPubMed
2.
go back to reference Popovic R, Liniger R, Bickler PE. Anesthetics and mild hypothermia similarly prevent hippocampal neuron death in an in vitro model of cerebral ischemia. Anesthesiology. 2000;92(5):1343–9.CrossRefPubMed Popovic R, Liniger R, Bickler PE. Anesthetics and mild hypothermia similarly prevent hippocampal neuron death in an in vitro model of cerebral ischemia. Anesthesiology. 2000;92(5):1343–9.CrossRefPubMed
3.
go back to reference Yon J-H, Daniel-Johnson J, Carter L, Jevtovic-Todorovic V. Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience. 2005;135(3):815–27.CrossRefPubMed Yon J-H, Daniel-Johnson J, Carter L, Jevtovic-Todorovic V. Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience. 2005;135(3):815–27.CrossRefPubMed
4.
go back to reference Cattano D, Williamson P, Fukui K, Avidan M, Evers AS, Olney JW, Young C. Potential of xenon to induce or to protect against neuroapoptosis in the developing mouse brain. Can J Anaesth. 2008;55(7):429–36.CrossRefPubMed Cattano D, Williamson P, Fukui K, Avidan M, Evers AS, Olney JW, Young C. Potential of xenon to induce or to protect against neuroapoptosis in the developing mouse brain. Can J Anaesth. 2008;55(7):429–36.CrossRefPubMed
5.
go back to reference Yang B, Liang G, Khojasteh S, Wu Z, Yang W, Joseph D, Wei H. Comparison of neurodegeneration and cognitive impairment in neonatal mice exposed to propofol or isoflurane. PLoS One. 2014;9(6):e99171.CrossRefPubMedPubMedCentral Yang B, Liang G, Khojasteh S, Wu Z, Yang W, Joseph D, Wei H. Comparison of neurodegeneration and cognitive impairment in neonatal mice exposed to propofol or isoflurane. PLoS One. 2014;9(6):e99171.CrossRefPubMedPubMedCentral
6.
go back to reference 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(3):876–82.PubMed 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(3):876–82.PubMed
7.
go back to reference Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev. 1979;3(1):79–83.CrossRefPubMed Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev. 1979;3(1):79–83.CrossRefPubMed
8.
go back to reference Grasshoff C, Rudolph U, Antkowiak B. Molecular and systemic mechanisms of general anaesthesia: the ‘multi-site and multiple mechanisms’ concept. Curr Opin Anaesthesiol. 2005;18(4):386–91.CrossRefPubMed Grasshoff C, Rudolph U, Antkowiak B. Molecular and systemic mechanisms of general anaesthesia: the ‘multi-site and multiple mechanisms’ concept. Curr Opin Anaesthesiol. 2005;18(4):386–91.CrossRefPubMed
10.
go back to reference Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Horster F, Tenkova T, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000;287(5455):1056–60.CrossRefPubMed Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Horster F, Tenkova T, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000;287(5455):1056–60.CrossRefPubMed
11.
go back to reference Zhang G, Dong Y, Zhang B, Ichinose F, Wu X, Culley DJ, Crosby G, Tanzi RE, Xie Z. Isoflurane-induced caspase-3 activation is dependent on cytosolic calcium and can be attenuated by memantine. J Neurosci. 2008;28(17):4551–60.CrossRefPubMedPubMedCentral Zhang G, Dong Y, Zhang B, Ichinose F, Wu X, Culley DJ, Crosby G, Tanzi RE, Xie Z. Isoflurane-induced caspase-3 activation is dependent on cytosolic calcium and can be attenuated by memantine. J Neurosci. 2008;28(17):4551–60.CrossRefPubMedPubMedCentral
13.
go back to reference Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16(3):1066–71.PubMed Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16(3):1066–71.PubMed
14.
go back to reference McCook O, Radermacher P, Volani C, Asfar P, Ignatius A, Kemmler J, Moller P, Szabo C, Whiteman M, Wood ME, et al. H2S during circulatory shock: some unresolved questions. Nitric Oxide. 2014;41:48–61.CrossRefPubMedPubMedCentral McCook O, Radermacher P, Volani C, Asfar P, Ignatius A, Kemmler J, Moller P, Szabo C, Whiteman M, Wood ME, et al. H2S during circulatory shock: some unresolved questions. Nitric Oxide. 2014;41:48–61.CrossRefPubMedPubMedCentral
15.
go back to reference Dorman DC, Moulin FJ, McManus BE, Mahle KC, James RA, Struve MF. Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci. 2002;65(1):18–25.CrossRefPubMed Dorman DC, Moulin FJ, McManus BE, Mahle KC, James RA, Struve MF. Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci. 2002;65(1):18–25.CrossRefPubMed
16.
go back to reference Hu LF, Lu M, Hon Wong PT, Bian JS. Hydrogen sulfide: neurophysiology and neuropathology. Antioxid Redox Signal. 2011;15(2):405–19.CrossRefPubMed Hu LF, Lu M, Hon Wong PT, Bian JS. Hydrogen sulfide: neurophysiology and neuropathology. Antioxid Redox Signal. 2011;15(2):405–19.CrossRefPubMed
17.
go back to reference Zhou CF, Tang XQ. Hydrogen sulfide and nervous system regulation. Chin Med J. 2011;124(21):3576–82.PubMed Zhou CF, Tang XQ. Hydrogen sulfide and nervous system regulation. Chin Med J. 2011;124(21):3576–82.PubMed
18.
go back to reference Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, Moore PK. Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol. 2006;149(6):625–34.CrossRefPubMedPubMedCentral Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, Moore PK. Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol. 2006;149(6):625–34.CrossRefPubMedPubMedCentral
19.
go back to reference Hu LF, Wong PT, Moore PK, Bian JS. Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem. 2007;100(4):1121–8.CrossRefPubMed Hu LF, Wong PT, Moore PK, Bian JS. Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem. 2007;100(4):1121–8.CrossRefPubMed
20.
go back to reference Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury--evidence for a role of K ATP channels. Basic Res Cardiol. 2006;101(1):53–60.CrossRefPubMed Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury--evidence for a role of K ATP channels. Basic Res Cardiol. 2006;101(1):53–60.CrossRefPubMed
21.
go back to reference Ali MY, Whiteman M, Low CM, Moore PK. Hydrogen sulphide reduces insulin secretion from HIT-T15 cells by a KATP channel-dependent pathway. J Endocrinol. 2007;195(1):105–12.CrossRefPubMed Ali MY, Whiteman M, Low CM, Moore PK. Hydrogen sulphide reduces insulin secretion from HIT-T15 cells by a KATP channel-dependent pathway. J Endocrinol. 2007;195(1):105–12.CrossRefPubMed
22.
go back to reference Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov. 2015;14(5):329–45.CrossRefPubMed Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov. 2015;14(5):329–45.CrossRefPubMed
23.
go back to reference Ma D, Williamson P, Januszewski A, et al. Xenon mitigates isoflurane-induced neuronal apoptosis in the developing rodent brain[J]. Anesthesiology: The Journal of the American Society of Anesthesiologists. 2007;106(4):746-53. Ma D, Williamson P, Januszewski A, et al. Xenon mitigates isoflurane-induced neuronal apoptosis in the developing rodent brain[J]. Anesthesiology: The Journal of the American Society of Anesthesiologists. 2007;106(4):746-53.
24.
go back to reference Robert D, Sanders BS. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats.Pdf. Anesthesiology. 2009;110:1077–85.CrossRef Robert D, Sanders BS. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats.Pdf. Anesthesiology. 2009;110:1077–85.CrossRef
25.
go back to reference Peng J, Drobish JK, Liang G, Wu Z, Liu C, Joseph DJ, Abdou H, Eckenhoff MF, Wei H. Anesthetic preconditioning inhibits isoflurane-mediated apoptosis in the developing rat brain. Anesth Analg. 2014;119(4):939–46.CrossRefPubMedPubMedCentral Peng J, Drobish JK, Liang G, Wu Z, Liu C, Joseph DJ, Abdou H, Eckenhoff MF, Wei H. Anesthetic preconditioning inhibits isoflurane-mediated apoptosis in the developing rat brain. Anesth Analg. 2014;119(4):939–46.CrossRefPubMedPubMedCentral
26.
go back to reference Paxinos G, Watson C, Petrides M, et al. The marmoset brain in stereotaxic coordinates[M]. San Diego: Elsevier Academic Press; 2012. Paxinos G, Watson C, Petrides M, et al. The marmoset brain in stereotaxic coordinates[M]. San Diego: Elsevier Academic Press; 2012.
27.
go back to reference Ansari B, Coates PJ, Greenstein BD, Hall PA. Situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol. 1993;170(1):1–8.CrossRefPubMed Ansari B, Coates PJ, Greenstein BD, Hall PA. Situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol. 1993;170(1):1–8.CrossRefPubMed
28.
go back to reference Vorhees CV, Williams MT. Value of water mazes for assessing spatial and egocentric learning and memory in rodent basic research and regulatory studies. Neurotoxicol Teratol. 2014;45:75–90.CrossRefPubMed Vorhees CV, Williams MT. Value of water mazes for assessing spatial and egocentric learning and memory in rodent basic research and regulatory studies. Neurotoxicol Teratol. 2014;45:75–90.CrossRefPubMed
29.
go back to reference 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(6):1325.CrossRefPubMedPubMedCentral 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(6):1325.CrossRefPubMedPubMedCentral
30.
go back to reference Jevtovic-Todorovic V, Absalom AR, Blomgren K, Brambrink A, Crosby G, Culley DJ, Fiskum G, Giffard RG, Herold KF, Loepke AW, et al. Anaesthetic neurotoxicity and neuroplasticity: an expert group report and statement based on the BJA Salzburg seminar. Br J Anaesth. 2013;111(2):143–51.CrossRefPubMedPubMedCentral Jevtovic-Todorovic V, Absalom AR, Blomgren K, Brambrink A, Crosby G, Culley DJ, Fiskum G, Giffard RG, Herold KF, Loepke AW, et al. Anaesthetic neurotoxicity and neuroplasticity: an expert group report and statement based on the BJA Salzburg seminar. Br J Anaesth. 2013;111(2):143–51.CrossRefPubMedPubMedCentral
31.
go back to reference Zhu C, Gao J, Karlsson N, Li Q, Zhang Y, Huang Z, Li H, Kuhn HG, Blomgren K. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab. 2010;30(5):1017–30.CrossRefPubMedPubMedCentral Zhu C, Gao J, Karlsson N, Li Q, Zhang Y, Huang Z, Li H, Kuhn HG, Blomgren K. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab. 2010;30(5):1017–30.CrossRefPubMedPubMedCentral
32.
go back to reference Jin Z, Chan H, Ning J, Lu K, Ma D. The role of hydrogen sulfide in pathologies of the vital organs and its clinical application. J Physiol Pharmacol. 2015;66(2):169–79.PubMed Jin Z, Chan H, Ning J, Lu K, Ma D. The role of hydrogen sulfide in pathologies of the vital organs and its clinical application. J Physiol Pharmacol. 2015;66(2):169–79.PubMed
33.
go back to reference Kimura Y, Dargusch R, Schubert D, Kimura H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal. 2006;8(3–4):661–70.CrossRefPubMed Kimura Y, Dargusch R, Schubert D, Kimura H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal. 2006;8(3–4):661–70.CrossRefPubMed
34.
go back to reference Tang G, Zhang L, Yang G, Wu L, Wang R. Hydrogen sulfide-induced inhibition of L-type Ca2+ channels and insulin secretion in mouse pancreatic beta cells. Diabetologia. 2013;56(3):533–41.CrossRefPubMed Tang G, Zhang L, Yang G, Wu L, Wang R. Hydrogen sulfide-induced inhibition of L-type Ca2+ channels and insulin secretion in mouse pancreatic beta cells. Diabetologia. 2013;56(3):533–41.CrossRefPubMed
35.
go back to reference Zhang R, Sun Y, Tsai H, Tang C, Jin H, Du J. Hydrogen sulfide inhibits L-type calcium currents depending upon the protein sulfhydryl state in rat cardiomyocytes. PLoS One. 2012;7(5):e37073.CrossRefPubMedPubMedCentral Zhang R, Sun Y, Tsai H, Tang C, Jin H, Du J. Hydrogen sulfide inhibits L-type calcium currents depending upon the protein sulfhydryl state in rat cardiomyocytes. PLoS One. 2012;7(5):e37073.CrossRefPubMedPubMedCentral
36.
go back to reference Garcia-Bereguiain MA, Samhan-Arias AK, Martin-Romero FJ, Gutierrez-Merino C. Hydrogen sulfide raises cytosolic calcium in neurons through activation of L-type Ca2+ channels. Antioxid Redox Signal. 2008;10(1):31–42.CrossRefPubMed Garcia-Bereguiain MA, Samhan-Arias AK, Martin-Romero FJ, Gutierrez-Merino C. Hydrogen sulfide raises cytosolic calcium in neurons through activation of L-type Ca2+ channels. Antioxid Redox Signal. 2008;10(1):31–42.CrossRefPubMed
37.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
38.
go back to reference Raines DE, Claycomb RJ, Forman SA. Modulation of GABA(A) receptor function by nonhalogenated alkane anesthetics: the effects on agonist enhancement, direct activation, and inhibition. Anesth Analg. 2003;96(1):112–8. table of contentsPubMed Raines DE, Claycomb RJ, Forman SA. Modulation of GABA(A) receptor function by nonhalogenated alkane anesthetics: the effects on agonist enhancement, direct activation, and inhibition. Anesth Analg. 2003;96(1):112–8. table of contentsPubMed
39.
go back to reference 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(6):4025–37.CrossRefPubMed 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(6):4025–37.CrossRefPubMed
40.
go back to reference Hu LF, Lu M, Z-Y W, Wong PT-H, Bian J-S. Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function. Mol Pharmacol. 2009;75(1):27–34.CrossRefPubMed Hu LF, Lu M, Z-Y W, Wong PT-H, Bian J-S. Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function. Mol Pharmacol. 2009;75(1):27–34.CrossRefPubMed
41.
go back to reference Łowicka E, Bełtowski J. Hydrogen sulfide (H2S)-the third gas of interest for pharmacologists. Pharmacol Rep. 2006;59(1):4–24. Łowicka E, Bełtowski J. Hydrogen sulfide (H2S)-the third gas of interest for pharmacologists. Pharmacol Rep. 2006;59(1):4–24.
42.
go back to reference Kimura Y, Goto Y-I, Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal. 2010;12(1):1–13.CrossRefPubMed Kimura Y, Goto Y-I, Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal. 2010;12(1):1–13.CrossRefPubMed
43.
go back to reference Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, Kevil CG, Lefer DJ. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res. 2009;105(4):365–74.CrossRefPubMedPubMedCentral Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, Kevil CG, Lefer DJ. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res. 2009;105(4):365–74.CrossRefPubMedPubMedCentral
44.
go back to reference Lu M, L-F H, Hu G, Bian J-S. Hydrogen sulfide protects astrocytes against H 2 O 2-induced neural injury via enhancing glutamate uptake. Free Radic Biol Med. 2008;45(12):1705–13.CrossRefPubMed Lu M, L-F H, Hu G, Bian J-S. Hydrogen sulfide protects astrocytes against H 2 O 2-induced neural injury via enhancing glutamate uptake. Free Radic Biol Med. 2008;45(12):1705–13.CrossRefPubMed
45.
go back to reference 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(3):1031–41.CrossRefPubMed 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(3):1031–41.CrossRefPubMed
46.
go back to reference Shao J-L, Wan X-H, Chen Y, Bi C, Chen H-M, Zhong Y, Heng X-H, Qian J-Q. H2S protects hippocampal neurons from anoxia–reoxygenation through cAMP-mediated PI3K/Akt/p70S6K cell-survival signaling pathways. J Mol Neurosci. 2011;43(3):453–60.CrossRefPubMed Shao J-L, Wan X-H, Chen Y, Bi C, Chen H-M, Zhong Y, Heng X-H, Qian J-Q. H2S protects hippocampal neurons from anoxia–reoxygenation through cAMP-mediated PI3K/Akt/p70S6K cell-survival signaling pathways. J Mol Neurosci. 2011;43(3):453–60.CrossRefPubMed
47.
go back to reference Giuliani D, Ottani A, Zaffe D, Galantucci M, Strinati F, Lodi R, Guarini S. Hydrogen sulfide slows down progression of experimental Alzheimer’s disease by targeting multiple pathophysiological mechanisms. Neurobiol Learn Mem. 2013;104:82–91.CrossRefPubMed Giuliani D, Ottani A, Zaffe D, Galantucci M, Strinati F, Lodi R, Guarini S. Hydrogen sulfide slows down progression of experimental Alzheimer’s disease by targeting multiple pathophysiological mechanisms. Neurobiol Learn Mem. 2013;104:82–91.CrossRefPubMed
48.
go back to reference Wu X, Lu Y, Dong Y, Zhang G, Zhang Y, Xu Z, Culley DJ, Crosby G, Marcantonio ER, Tanzi RE. The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-α, IL-6, and IL-1β. Neurobiol Aging. 2012;33(7):1364–78.CrossRefPubMed Wu X, Lu Y, Dong Y, Zhang G, Zhang Y, Xu Z, Culley DJ, Crosby G, Marcantonio ER, Tanzi RE. The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-α, IL-6, and IL-1β. Neurobiol Aging. 2012;33(7):1364–78.CrossRefPubMed
49.
go back to reference Eto K, Asada T, Arima K, Makifuchi T, Kimura H. Brain hydrogen sulfide is severely decreased in Alzheimer's disease. Biochem Biophys Res Commun. 2002;293(5):1485–8.CrossRefPubMed Eto K, Asada T, Arima K, Makifuchi T, Kimura H. Brain hydrogen sulfide is severely decreased in Alzheimer's disease. Biochem Biophys Res Commun. 2002;293(5):1485–8.CrossRefPubMed
50.
go back to reference Wen X, Qi D, Sun Y, Huang X, Zhang F, Wu J, Fu Y, Ma K, Du Y, Dong H, et al. H(2)S attenuates cognitive deficits through Akt1/JNK3 signaling pathway in ischemic stroke. Behav Brain Res. 2014;269:6–14.CrossRefPubMed Wen X, Qi D, Sun Y, Huang X, Zhang F, Wu J, Fu Y, Ma K, Du Y, Dong H, et al. H(2)S attenuates cognitive deficits through Akt1/JNK3 signaling pathway in ischemic stroke. Behav Brain Res. 2014;269:6–14.CrossRefPubMed
51.
go back to reference Chu QJ, He L, Zhang W, Liu CL, Ai YQ, Zhang Q. Hydrogen sulfide attenuates surgical trauma-induced inflammatory response and cognitive deficits in mice. J Surg Res. 2013;183(1):330–6.CrossRefPubMed Chu QJ, He L, Zhang W, Liu CL, Ai YQ, Zhang Q. Hydrogen sulfide attenuates surgical trauma-induced inflammatory response and cognitive deficits in mice. J Surg Res. 2013;183(1):330–6.CrossRefPubMed
52.
go back to reference Fournier NM, Calverley KL, Wagner JP, Poock JL, Crossley M. Impaired social cognition 30 years after hemispherectomy for intractable epilepsy: the importance of the right hemisphere in complex social functioning. Epilepsy Behav. 2008;12(3):460–71.CrossRefPubMed Fournier NM, Calverley KL, Wagner JP, Poock JL, Crossley M. Impaired social cognition 30 years after hemispherectomy for intractable epilepsy: the importance of the right hemisphere in complex social functioning. Epilepsy Behav. 2008;12(3):460–71.CrossRefPubMed
53.
go back to reference Kuan CY, Roth KA, Flavell RA, Rakic P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 2000;23(7):291–7.CrossRefPubMed Kuan CY, Roth KA, Flavell RA, Rakic P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 2000;23(7):291–7.CrossRefPubMed
54.
go back to reference Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C, Roth KA. Ethanol-induced caspase-3 activation in the in vivo developing mouse brain. Neurobiol Dis. 2002;9(2):205–19.CrossRefPubMed Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C, Roth KA. Ethanol-induced caspase-3 activation in the in vivo developing mouse brain. Neurobiol Dis. 2002;9(2):205–19.CrossRefPubMed
55.
go back to reference Arkhipov V. Memory dissociation: the approach to the study of retrieval processes. Behav Brain Res. 1999;106(1):39–46.CrossRefPubMed Arkhipov V. Memory dissociation: the approach to the study of retrieval processes. Behav Brain Res. 1999;106(1):39–46.CrossRefPubMed
56.
go back to reference Nagpure BV, Bian JS. Brain, learning, and memory: role of H2S in neurodegenerative diseases. Handb Exp Pharmacol. 2015;230:193–215.CrossRefPubMed Nagpure BV, Bian JS. Brain, learning, and memory: role of H2S in neurodegenerative diseases. Handb Exp Pharmacol. 2015;230:193–215.CrossRefPubMed
Metadata
Title
Hydrogen sulfide attenuates isoflurane-induced neuroapoptosis and cognitive impairment in the developing rat brain
Authors
Xueyuan Hu
Li Luan
Wei Guan
Shuai Zhang
Bei Li
Wei Ji
Honggang Fan
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Anesthesiology / Issue 1/2017
Electronic ISSN: 1471-2253
DOI
https://doi.org/10.1186/s12871-017-0419-y

Other articles of this Issue 1/2017

BMC Anesthesiology 1/2017 Go to the issue