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Erschienen in: Journal of Anesthesia 6/2023

22.08.2023 | Original Article

Proteomic analysis of gene expression in the prefrontal cortex in infant rhesus macaques after multiple sevoflurane exposures

verfasst von: Lingling Shi, Zhenyu Xue, Haoli Mao, Hong Jiang, Lei Zhang

Erschienen in: Journal of Anesthesia | Ausgabe 6/2023

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Abstract

Purpose

Repeated exposure of infant rhesus macaques to sevoflurane induces neurotoxicity and is associated with neurocognitive impairment in later life. We aimed to investigate the effect of repeated sevoflurane exposure on the expression of proteins in the prefrontal cortex of infant rhesus macaques by proteomics.

Methods

Rhesus macaques were exposed to sevoflurane three times, on postnatal days 7, 21 and 35. Quantitative proteomics employing LC–MS with isobaric labeling (TMT10plex), western blotting, and transmission electron microscopy (TEM) were utilized in the studies.

Results

The results of a proteomics investigation of the brain revealed that the proteins that were differentially expressed in rhesus macaques after sevoflurane exposures were associated mainly with mitochondrial respiration. Following multiple sevoflurane exposures, the prefrontal cortices of rhesus macaques exhibited increases in NDUFA8 and COX IV protein levels, while no alterations in mitochondrial morphology were observed through TEM.

Conclusion

Multiple exposures to sevoflurane increased the mitochondrial protein levels in rhesus macaques.
Literatur
1.
Zurück zum Zitat Walkden GJ, Gill H, Davies NM, Peters AE, Wright I, Pickering AE. Early childhood general anesthesia and neurodevelopmental outcomes in the Avon Longitudinal Study of parents and children birth cohort. Anesthesiology. 2020;133:1007–20.CrossRefPubMed Walkden GJ, Gill H, Davies NM, Peters AE, Wright I, Pickering AE. Early childhood general anesthesia and neurodevelopmental outcomes in the Avon Longitudinal Study of parents and children birth cohort. Anesthesiology. 2020;133:1007–20.CrossRefPubMed
2.
Zurück zum Zitat Alvarado MC, Murphy KL, Baxter MG. Visual recognition memory is impaired in rhesus monkeys repeatedly exposed to sevoflurane in infancy. Br J Anaesth. 2017;119:517–23.CrossRefPubMedPubMedCentral Alvarado MC, Murphy KL, Baxter MG. Visual recognition memory is impaired in rhesus monkeys repeatedly exposed to sevoflurane in infancy. Br J Anaesth. 2017;119:517–23.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Fehr T, Janssen WGM, Park J, Baxter MG. Neonatal exposures to sevoflurane in rhesus monkeys alter synaptic ultrastructure in later life. iScience. 2022;25:105685.CrossRefPubMedPubMedCentral Fehr T, Janssen WGM, Park J, Baxter MG. Neonatal exposures to sevoflurane in rhesus monkeys alter synaptic ultrastructure in later life. iScience. 2022;25:105685.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Xie L, Liu Y, Hu Y, Wang B, Zhu Z, Jiang Y, Suo Y, Hu M, Gao J, Ullah R, Hu Z. Neonatal sevoflurane exposure induces impulsive behavioral deficit through disrupting excitatory neurons in the medial prefrontal cortex in mice. Transl Psychiatry. 2020;10:202.CrossRefPubMedPubMedCentral Xie L, Liu Y, Hu Y, Wang B, Zhu Z, Jiang Y, Suo Y, Hu M, Gao J, Ullah R, Hu Z. Neonatal sevoflurane exposure induces impulsive behavioral deficit through disrupting excitatory neurons in the medial prefrontal cortex in mice. Transl Psychiatry. 2020;10:202.CrossRefPubMedPubMedCentral
5.
6.
Zurück zum Zitat Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167–202.CrossRefPubMed Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167–202.CrossRefPubMed
7.
Zurück zum Zitat Xu X, Tian X, Wang G. Sevoflurane reduced functional connectivity of excitatory neurons in prefrontal cortex during working memory performance of aged rats. Biomed Pharmacother. 2018;106:1258–66.CrossRefPubMed Xu X, Tian X, Wang G. Sevoflurane reduced functional connectivity of excitatory neurons in prefrontal cortex during working memory performance of aged rats. Biomed Pharmacother. 2018;106:1258–66.CrossRefPubMed
8.
Zurück zum Zitat Zhao T, Chen Y, Sun Z, Shi Z, Qin J, Lu J, Li C, Ma D, Zhou L, Song X. Prenatal sevoflurane exposure causes neuronal excitatory/inhibitory imbalance in the prefrontal cortex and neurofunctional abnormality in rats. Neurobiol Dis. 2020;146: 105121.CrossRefPubMed Zhao T, Chen Y, Sun Z, Shi Z, Qin J, Lu J, Li C, Ma D, Zhou L, Song X. Prenatal sevoflurane exposure causes neuronal excitatory/inhibitory imbalance in the prefrontal cortex and neurofunctional abnormality in rats. Neurobiol Dis. 2020;146: 105121.CrossRefPubMed
9.
Zurück zum Zitat Song R, Ling X, Peng M, Xue Z, Cang J, Fang F. Maternal sevoflurane exposure causes abnormal development of fetal prefrontal cortex and induces cognitive dysfunction in offspring. Stem Cells Int. 2017;2017:6158468.CrossRefPubMedPubMedCentral Song R, Ling X, Peng M, Xue Z, Cang J, Fang F. Maternal sevoflurane exposure causes abnormal development of fetal prefrontal cortex and induces cognitive dysfunction in offspring. Stem Cells Int. 2017;2017:6158468.CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Cabral-Costa JV, Kowaltowski AJ. Neurological disorders and mitochondria. Mol Aspects Med. 2020;71: 100826.CrossRefPubMed Cabral-Costa JV, Kowaltowski AJ. Neurological disorders and mitochondria. Mol Aspects Med. 2020;71: 100826.CrossRefPubMed
11.
Zurück zum Zitat Qi J, Jia Y, Wang W, Lu H, Wang Y, Li Z. The role of Bag2 in neurotoxicity induced by the anesthetic sevoflurane. J Cell Biochem. 2018;120:7551.CrossRefPubMed Qi J, Jia Y, Wang W, Lu H, Wang Y, Li Z. The role of Bag2 in neurotoxicity induced by the anesthetic sevoflurane. J Cell Biochem. 2018;120:7551.CrossRefPubMed
12.
Zurück zum Zitat Zhu X, Yao Y, Guo M, Li J, Yang P, Xu H, Lin D. Sevoflurane increases intracellular calcium to induce mitochondrial injury and neuroapoptosis. Toxicol Lett. 2021;336:11–20.CrossRefPubMed Zhu X, Yao Y, Guo M, Li J, Yang P, Xu H, Lin D. Sevoflurane increases intracellular calcium to induce mitochondrial injury and neuroapoptosis. Toxicol Lett. 2021;336:11–20.CrossRefPubMed
13.
Zurück zum Zitat Chen Y, Zhang P, Lin X, Zhang H, Miao J, Zhou Y, Chen G. Mitophagy impairment is involved in sevoflurane-induced cognitive dysfunction in aged rats. Aging (Albany NY). 2020;12:17235–56.CrossRefPubMed Chen Y, Zhang P, Lin X, Zhang H, Miao J, Zhou Y, Chen G. Mitophagy impairment is involved in sevoflurane-induced cognitive dysfunction in aged rats. Aging (Albany NY). 2020;12:17235–56.CrossRefPubMed
14.
Zurück zum Zitat Raper J, Alvarado MC, Murphy KL, Baxter MG. Multiple anesthetic exposure in infant monkeys alters emotional reactivity to an acute stressor. Anesthesiology. 2015;123:1084–92.CrossRefPubMed Raper J, Alvarado MC, Murphy KL, Baxter MG. Multiple anesthetic exposure in infant monkeys alters emotional reactivity to an acute stressor. Anesthesiology. 2015;123:1084–92.CrossRefPubMed
15.
Zurück zum Zitat Zhang L, Xue Z, Liu Q, Liu Y, Xi S, Cheng Y, Li J, Yan J, Shen Y, Xiao C, Xie Z, Qiu Z, Jiang H. Disrupted folate metabolism with anesthesia leads to myelination deficits mediated by epigenetic regulation of ERMN. EBioMedicine. 2019;43:473–86.CrossRefPubMedPubMedCentral Zhang L, Xue Z, Liu Q, Liu Y, Xi S, Cheng Y, Li J, Yan J, Shen Y, Xiao C, Xie Z, Qiu Z, Jiang H. Disrupted folate metabolism with anesthesia leads to myelination deficits mediated by epigenetic regulation of ERMN. EBioMedicine. 2019;43:473–86.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.CrossRefPubMedPubMedCentral Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering CV. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607-d613.CrossRefPubMed Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering CV. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607-d613.CrossRefPubMed
18.
Zurück zum Zitat Thompson K, Collier JJ, Glasgow RIC, Robertson FM, Pyle A, Blakely EL, Alston CL, Oláhová M, McFarland R, Taylor RW. Recent advances in understanding the molecular genetic basis of mitochondrial disease. J Inherit Metab Dis. 2020;43:36–50.CrossRefPubMed Thompson K, Collier JJ, Glasgow RIC, Robertson FM, Pyle A, Blakely EL, Alston CL, Oláhová M, McFarland R, Taylor RW. Recent advances in understanding the molecular genetic basis of mitochondrial disease. J Inherit Metab Dis. 2020;43:36–50.CrossRefPubMed
19.
Zurück zum Zitat Vos M, Esposito G, Edirisinghe JN, Vilain S, Haddad DM, Slabbaert JR, Van Meensel S, Schaap O, De Strooper B, Meganathan R, Morais VA, Verstreken P. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science. 2012;336:1306–10.CrossRefPubMed Vos M, Esposito G, Edirisinghe JN, Vilain S, Haddad DM, Slabbaert JR, Van Meensel S, Schaap O, De Strooper B, Meganathan R, Morais VA, Verstreken P. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science. 2012;336:1306–10.CrossRefPubMed
20.
Zurück zum Zitat Ye Z, Xia P, Cheng ZG, Guo Q. Neuroprotection induced by sevoflurane-delayed post-conditioning is attributable to increased phosphorylation of mitochondrial GSK-3β through the PI3K/Akt survival pathway. J Neurol Sci. 2015;348:216–25.CrossRefPubMed Ye Z, Xia P, Cheng ZG, Guo Q. Neuroprotection induced by sevoflurane-delayed post-conditioning is attributable to increased phosphorylation of mitochondrial GSK-3β through the PI3K/Akt survival pathway. J Neurol Sci. 2015;348:216–25.CrossRefPubMed
21.
Zurück zum Zitat Ogilvie I, Kennaway NG, Shoubridge EA. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J Clin Invest. 2005;115:2784–92.CrossRefPubMedPubMedCentral Ogilvie I, Kennaway NG, Shoubridge EA. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J Clin Invest. 2005;115:2784–92.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Burman JL, Itsara LS, Kayser EB, Suthammarak W, Wang AM, Kaeberlein M, Sedensky MM, Morgan PG, Pallanck LJ. A Drosophila model of mitochondrial disease caused by a complex I mutation that uncouples proton pumping from electron transfer. Dis Model Mech. 2014;7:1165–74.PubMedPubMedCentral Burman JL, Itsara LS, Kayser EB, Suthammarak W, Wang AM, Kaeberlein M, Sedensky MM, Morgan PG, Pallanck LJ. A Drosophila model of mitochondrial disease caused by a complex I mutation that uncouples proton pumping from electron transfer. Dis Model Mech. 2014;7:1165–74.PubMedPubMedCentral
23.
Zurück zum Zitat Wiedemann N, Frazier AE, Pfanner N. The protein import machinery of mitochondria. J Biol Chem. 2004;279:14473–6.CrossRefPubMed Wiedemann N, Frazier AE, Pfanner N. The protein import machinery of mitochondria. J Biol Chem. 2004;279:14473–6.CrossRefPubMed
24.
Zurück zum Zitat Sprenger HG, Langer T. The good and the bad of mitochondrial breakups. Trends Cell Biol. 2019;29:888–900.CrossRefPubMed Sprenger HG, Langer T. The good and the bad of mitochondrial breakups. Trends Cell Biol. 2019;29:888–900.CrossRefPubMed
25.
Zurück zum Zitat Shan Y, Sun S, Yang F, Shang N, Liu H. Dexmedetomidine protects the developing rat brain against the neurotoxicity wrought by sevoflurane: role of autophagy and Drp1-Bax signaling. Drug Des Devel Ther. 2018;12:3617–24.CrossRefPubMedPubMedCentral Shan Y, Sun S, Yang F, Shang N, Liu H. Dexmedetomidine protects the developing rat brain against the neurotoxicity wrought by sevoflurane: role of autophagy and Drp1-Bax signaling. Drug Des Devel Ther. 2018;12:3617–24.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Ye JS, Chen L, Lu YY, Lei SQ, Peng M, Xia ZY. Honokiol-Mediated mitophagy ameliorates postoperative cognitive impairment induced by surgery/sevoflurane via inhibiting the activation of NLRP3 inflammasome in the hippocampus. Oxid Med Cell Longev. 2019;2019:8639618.CrossRefPubMedPubMedCentral Ye JS, Chen L, Lu YY, Lei SQ, Peng M, Xia ZY. Honokiol-Mediated mitophagy ameliorates postoperative cognitive impairment induced by surgery/sevoflurane via inhibiting the activation of NLRP3 inflammasome in the hippocampus. Oxid Med Cell Longev. 2019;2019:8639618.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Zhang L, Mao H, Yan J, Cheng Y, Xue Z, Qiu Z, Jiang H. Sevoflurane enhances brain glycolysis and lactate production in aged marmosets. Br J Anaesth. 2022;129:63–6.CrossRef Zhang L, Mao H, Yan J, Cheng Y, Xue Z, Qiu Z, Jiang H. Sevoflurane enhances brain glycolysis and lactate production in aged marmosets. Br J Anaesth. 2022;129:63–6.CrossRef
Metadaten
Titel
Proteomic analysis of gene expression in the prefrontal cortex in infant rhesus macaques after multiple sevoflurane exposures
verfasst von
Lingling Shi
Zhenyu Xue
Haoli Mao
Hong Jiang
Lei Zhang
Publikationsdatum
22.08.2023
Verlag
Springer Nature Singapore
Erschienen in
Journal of Anesthesia / Ausgabe 6/2023
Print ISSN: 0913-8668
Elektronische ISSN: 1438-8359
DOI
https://doi.org/10.1007/s00540-023-03244-x

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