Sub-dose anesthetics combined with chloride regulators protect the brain against chronic ischemia-hypoxia injury.

chloride ion cognitive function hypoxia ischemia propofol sevoflurane γ-Aminobutyric acid

Journal

CNS neuroscience & therapeutics
ISSN: 1755-5949
Titre abrégé: CNS Neurosci Ther
Pays: England
ID NLM: 101473265

Informations de publication

Date de publication:
06 Aug 2023
Historique:
revised: 11 07 2023
received: 07 01 2022
accepted: 13 07 2023
medline: 7 8 2023
pubmed: 7 8 2023
entrez: 6 8 2023
Statut: aheadofprint

Résumé

Cerebral ischemia-hypoxia leads to excitotoxicity-mediated neuronal damage and cognitive dysfunction, especially in the elderly. Excessive intracellular [Cl Chronic cerebral hypoxia (CCH) model was established by bilateral carotid artery ligation in aged rats. Sub-dose of anesthetics (propofol and sevoflurane) with or without KCC2 agonist N-ethylmaleimide (NEM) or Na Sub-anesthetic dose of combined propofol (1.2 μg mL Sub-anesthetic dose of propofol and sevoflurane is a recommended anesthesia regimen in at-risk patients. Restoration of [Cl

Sections du résumé

BACKGROUND BACKGROUND
Cerebral ischemia-hypoxia leads to excitotoxicity-mediated neuronal damage and cognitive dysfunction, especially in the elderly. Excessive intracellular [Cl
METHODS METHODS
Chronic cerebral hypoxia (CCH) model was established by bilateral carotid artery ligation in aged rats. Sub-dose of anesthetics (propofol and sevoflurane) with or without KCC2 agonist N-ethylmaleimide (NEM) or Na
RESULTS RESULTS
Sub-anesthetic dose of combined propofol (1.2 μg mL
CONCLUSION CONCLUSIONS
Sub-anesthetic dose of propofol and sevoflurane is a recommended anesthesia regimen in at-risk patients. Restoration of [Cl

Identifiants

pubmed: 37545014
doi: 10.1111/cns.14379
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 82071220
Organisme : Natural Science Foundation of Tianjin City
ID : 20JCYBJC01290
Organisme : Science and Technology Foundation of Tianjin Health Commission
ID : MS20013
Organisme : Tianjin key Medical Discipline (Specialty) Construction Project.
ID : TJYXZDXK-072C
Organisme : Tianjin Multiple Investment Foundation of Applied Basic Research
ID : 21JCQNJC01020

Informations de copyright

© 2023 The Authors. CNS Neuroscience & Therapeutics Published by John Wiley & Sons Ltd.

Références

Rius-Pérez S, Tormos AM, Pérez S, Taléns-Visconti R. Vascular pathology: cause or effect in Alzheimer disease? Neurologia. 2018;33:112-120.
Bandera E, Botteri M, Minelli C, Sutton A, Abrams KR, Latronico N. Cerebral blood flow threshold of ischemic penumbra and infarct core in acute ischemic stroke: a systematic review. Stroke. 2006;37:1334-1339.
Zhu H, Yoshimoto T, Imajo-Ohmi S, Dazortsava M, Mathivanan A, Yamashima T. Why are hippocampal CA1 neurons vulnerable but motor cortex neurons resistant to transient ischemia? J Neurochem. 2012;120:574-585.
Matveychuk D, MacKenzie EM, Kumpula D, et al. Overview of the neuroprotective effects of the MAO-inhibiting antidepressant phenelzine. Cell Mol Neurobiol. 2021;42:225-242.
Gamba G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev. 2005;85:423-493.
Russell JM. Sodium-potassium-chloride cotransport. Physiol Rev. 2000;80:211-276.
Chinn GA, Sasaki Russell JM, Yabut NA, Maharjan D, Sall JW. Androgenic modulation of the chloride transporter NKCC1 contributes to age-dependent isoflurane neurotoxicity in male rats. Anesthesiology. 2020;133:852-866.
Bi D, Wen L, Wu Z, Shen Y. GABAergic dysfunction in excitatory and inhibitory (E/I) imbalance drives the pathogenesis of Alzheimer's disease. Alzheimers Dement. 2020;16:1312-1329.
Pozzi D, Rasile M, Corradini I, Matteoli M. Environmental regulation of the chloride transporter KCC2: switching inflammation off to switch the GABA on? Transl Psychiatry. 2020;10:349.
Engin E, Benham RS, Rudolph U. An emerging circuit pharmacology of GABA receptors. Trends Pharmacol Sci. 2018;39:710-732.
Liu L, Li C-j, Lu Y, et al. Baclofen mediates neuroprotection on hippocampal CA1 pyramidal cells through the regulation of autophagy under chronic cerebral hypoperfusion. Sci Rep. 2015;5:14474.
Zhao Z-F, Du L, Gao T, et al. Inhibition of α5 GABAA receptors has preventive but not therapeutic effects on isoflurane-induced memory impairment in aged rats. Neural Regen Res. 2019;14:1029-1036.
Bu X, Li T, Wang H, et al. Combination of isoflurane and propofol as general anesthesia during orthopedic surgery of perioperative cerebral hypoperfusion rats to avoid cognitive impairment. Front Med. 2020;7:549081.
Brioni JD, Varughese S, Ahmed R, Bein B. A clinical review of inhalation anesthesia with sevoflurane: from early research to emerging topics. J Anesth. 2017;31:764-778.
Wang H, Liu S, Wang H, Wang G, Zhu A. The effect of propofol postconditioning on the expression of K(+)-Cl(−)-co-transporter 2 in GABAergic inhibitory interneurons of acute ischemia/reperfusion injury rats. Brain Res. 2015;1597:210-219.
Yang C-Y, Liu S-Y, Wang H-Y, et al. Neuroprotection by propofol post-conditioning: focus on PKMζ/KCC2 pathway activity. Cell Mol Neurobiol. 2018;38:691-701.
Mitroshina ЕV, Mishchenko TA, Usenko AV, et al. AAV-syn-BDNF-EGFP virus construct exerts neuroprotective action on the hippocampal neural network during hypoxia in vitro. Int J Mol Sci. 2018;19:19.
Turovskaya MV, Gaidin SG, Vedunova MV, Babaev AA, Turovsky EA. BDNF overexpression enhances the preconditioning effect of brief episodes of hypoxia, promoting survival of GABAergic neurons. Neurosci Bull. 2020;36:733-760.
Ben-Ari Y. NKCC1 chloride importer antagonists attenuate many neurological and psychiatric disorders. Trends Neurosci. 2017;40:536-554.
Conway LC, Cardarelli RA, Moore YE, et al. Ethylmaleimide increases KCC2 cotransporter activity by modulating transporter phosphorylation. J Biol Chem. 2017;292:21253-21263.
Brewer GJ, Torricelli JR. Isolation and culture of adult neurons and neurospheres. Nat Protoc. 2007;2:1490-1498.
Hofmeijer J, Mulder ATB, Farinha AC, van Putten MJAM, le Feber J. Mild hypoxia affects synaptic connectivity in cultured neuronal networks. Brain Res. 2014;1557:180-189.
Perry JSA, Morioka S, Medina CB, et al. Interpreting an apoptotic corpse as anti-inflammatory involves a chloride sensing pathway. Nat Cell Biol. 2019;21:1532-1543.
Wang J, Yang C, Wang H, et al. A new rat model of chronic cerebral hypoperfusion resulting in early-stage vascular cognitive impairment. Front Aging Neurosci. 2020;12:86.
Lu K-T, Wu C-Y, Cheng N-C, et al. Inhibition of the Na+ -K+ -2Cl- -cotransporter in choroid plexus attenuates traumatic brain injury-induced brain edema and neuronal damage. Eur J Pharmacol. 2006;548:548-105.
O'Donnell ME, Tran L, Lam TI, Liu XB, Anderson SE. Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cerebral Blood Flow Metabol. 2004;24:1046-1056.
Sánchez-Mendoza ME, López-Lorenzo Y, Cruz-Antonio L, Cruz-Oseguera A, García-Machorro J, Arrieta J. Gastroprotective effect of Juanislamin on ethanol-induced gastric lesions in rats: role of prostaglandins, nitric oxide and sulfhydryl groups in the mechanism of action. Molecules. 2020;25:2246.
Yamamoto H, Okada N, Yano I, Murano T. Studies on pharmacodynamic action of N-ethylmaleimide (NEM). 2. An inflammatory property of NEM in rats. Jpn J Pharmacol. 1973;23:161-166.
Korol SV, Tafreshiha A, Bhandage AK, Birnir B, Jin Z. Insulin enhances GABA receptor-mediated inhibitory currents in rat central amygdala neurons. Neurosci Lett. 2018;671:76-81.
Iadecola C, Duering M, Hachinski V, et al. Vascular cognitive impairment and dementia: JACC scientific expert panel. J Am Coll Cardiol. 2019;73:3326-3344.
Belrose JC, Noppens RR. Anesthesiology and cognitive impairment: a narrative review of current clinical literature. BMC Anesthesiol. 2019;19:241.
Mahli A, Coskun D, Karaca GI, Akcali DT, Karabiyik L, Karadenizli Y. Target-controlled infusion of remifentanil with propofol or desflurane under bispectral index guidance: quality of anesthesia and recovery profile. J Res Med Sci. 2011;16:611-620.
Logginidou HG, Li B-H, Li D-P, et al. Propofol suppresses the cortical somatosensory evoked potential in rats. Anesth Analg. 2003;97:1784-1788.
Wang H-y, Wang G-l, Yu Y-h, Wang Y. The role of phosphoinositide-3-kinase/Akt pathway in propofol-induced postconditioning against focal cerebral ischemia-reperfusion injury in rats. Brain Res. 2009;1297:177-184.
Thal SC, Timaru-Kast R, Wilde F, et al. Propofol impairs neurogenesis and neurologic recovery and increases mortality rate in adult rats after traumatic brain injury. Crit Care Med. 2014;42:129-141.
Gómez de Segura IA, de la Vibora JB, Aguado D. Opioid tolerance blunts the reduction in the sevoflurane minimum alveolar concentration produced by remifentanil in the rat. Anesthesiology. 2009;110:1133-1138.
Zhang D-X, Jiang S, Yu L-N, Zhang F-J, Zhuang Q, Yan M. The effect of sevoflurane on the cognitive function of rats and its association with the inhibition of synaptic transmission. Int J Clin Exp Med. 2015;8:20853-20860.
Tian Y, Chen K-Y, Liu L-D, Dong Y-X, Zhao P, Guo S-B. Sevoflurane exacerbates cognitive impairment induced by a in rats through initiating neurotoxicity, neuroinflammation, and neuronal apoptosis in rat hippocampus. Mediators Inflamm. 2018;2018:3802324.
Bu X, Li T, Guo D, et al. 1% isoflurane and 1.2 μg/ml of propofol: a combination of anesthetics that causes the least damage to hypoxic neurons. Front Aging Neurosci. 2020;12:591938.
Johnston MV, Trescher WH, Ishida A, Nakajima W. Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res. 2001;49:735-741.
Edwards AB, Anderton RS, Knuckey NW, Meloni BP. Perinatal hypoxic-ischemic encephalopathy and neuroprotective peptide therapies: a case for cationic arginine-rich peptides (CARPs). Brain Sci. 2018;8:8.
Blauwblomme T, Dzhala V, Staley K. Transient ischemia facilitates neuronal chloride accumulation and severity of seizures. Annals Clin Transl Neurol. 2018;5:1048-1061.
Allen NJ, Rossi DJ, Attwell D. Sequential release of GABA by exocytosis and reversed uptake leads to neuronal swelling in simulated ischemia of hippocampal slices. J Neurosci. 2004;24:3837-3849.
Gao TM, Pulsinelli WA, Xu ZC. Changes in membrane properties of CA1 pyramidal neurons after transient forebrain ischemia in vivo. Neuroscience. 1999;90:771-780.
Xie S, Yu L, Zhou M, Liu L, Lei D, Han C. Association between BDNF rs6265 polymorphisms and postoperative cognitive dysfunction in Chinese Han population. Brain Behavior. 2020;10:e01800.
Qiu L-L, Pan W, Luo D, et al. Dysregulation of BDNF/TrkB signaling mediated by NMDAR/Ca/calpain might contribute to postoperative cognitive dysfunction in aging mice. J Neuroinflammation. 2020;17:23.
Reichardt LF. Neurotrophin-regulated signalling pathways. Philosophical transactions of the Royal Society of London. Series B. Biol Sci. 2006;361:1545-1564.
Ludwig A, Uvarov P, Soni S, Thomas-Crusells J, Airaksinen MS, Rivera C. Early growth response 4 mediates BDNF induction of potassium chloride cotransporter 2 transcription. J Neurosci. 2011;31:644-649.
Szymanski J, Minichiello L. NKCC1 deficiency in forming hippocampal circuits triggers neurodevelopmental disorder: role of BDNF-TrkB Signalling. Brain Sci. 2022;12:12.
Hu J-J, Yang X-L, Luo W-D, et al. Bumetanide reduce the seizure susceptibility induced by pentylenetetrazol via inhibition of aberrant hippocampal neurogenesis in neonatal rats after hypoxia-ischemia. Brain Res Bull. 2017;130:188-199.
Taubes A, Nova P, Zalocusky KA, et al. Experimental and real-world evidence supporting the computational repurposing of bumetanide for APOE4-related Alzheimer's disease. Nat Aging. 2021;1:932-947.
Heubl M, Zhang J, Pressey JC, et al. GABA receptor dependent synaptic inhibition rapidly tunes KCC2 activity via the Cl-sensitive WNK1 kinase. Nat Commun. 2017;8:1776.
Lombardi A, Jedlicka P, Luhmann HJ, Kilb W. Interactions between membrane resistance, GABA-A receptor properties, bicarbonate dynamics and Cl-transport shape activity-dependent changes of intracellular Cl concentration. Int J Mol Sci. 2019;20:20.
Cikic S, Chandra PK, Harman JC, et al. Sexual differences in mitochondrial and related proteins in rat cerebral microvessels: a proteomic approach. J Cerebral Blood Flow Metabol. 2021;41:397-412.
Wang R, Oh JM, Motovylyak A, et al. Impact of sex and APOE ε4 on age-related cerebral perfusion trajectories in cognitively asymptomatic middle-aged and older adults: a longitudinal study. J Cerebral Blood Flow Metabol. 2021;41:3016-3027.
Chandra PK, Cikic S, Baddoo MC, et al. Transcriptome analysis reveals sexual disparities in gene expression in rat brain microvessels. J Cerebral Blood Flow Metabol. 2021;41:2311-2328.

Auteurs

Chenyi Yang (C)

Nankai University, Tianjin, China.
Nankai University Affinity the Third Central Hospital, Tianjin, China.
The Third Central Clinical College of Tianjin Medical University, Tianjin, China.
Tianjin Key Laboratory of Extracorporeal Life Support for Critical Diseases, Tianjin, China.
Artificial Cell Engineering Technology Research Center, Tianjin, China.
Tianjin Institute of Hepatobiliary Disease, Tianjin, China.

Ye Wang (Y)

The Third Central Clinical College of Tianjin Medical University, Tianjin, China.

Yun Li (Y)

The Third Central Clinical College of Tianjin Medical University, Tianjin, China.

Xinyi Wang (X)

Nankai University Affinity the Third Central Hospital, Tianjin, China.
The Third Central Clinical College of Tianjin Medical University, Tianjin, China.
Tianjin Key Laboratory of Extracorporeal Life Support for Critical Diseases, Tianjin, China.
Artificial Cell Engineering Technology Research Center, Tianjin, China.
Tianjin Institute of Hepatobiliary Disease, Tianjin, China.

Wei Hua (W)

Nankai University Affinity the Third Central Hospital, Tianjin, China.
The Third Central Clinical College of Tianjin Medical University, Tianjin, China.
Tianjin Key Laboratory of Extracorporeal Life Support for Critical Diseases, Tianjin, China.
Artificial Cell Engineering Technology Research Center, Tianjin, China.
Tianjin Institute of Hepatobiliary Disease, Tianjin, China.

Zhuo Yang (Z)

Nankai University, Tianjin, China.

Haiyun Wang (H)

Nankai University, Tianjin, China.
Nankai University Affinity the Third Central Hospital, Tianjin, China.
The Third Central Clinical College of Tianjin Medical University, Tianjin, China.
Tianjin Key Laboratory of Extracorporeal Life Support for Critical Diseases, Tianjin, China.
Artificial Cell Engineering Technology Research Center, Tianjin, China.
Tianjin Institute of Hepatobiliary Disease, Tianjin, China.

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