Sevoflurane Postconditioning Ameliorates Neuronal Migration Disorder Through Reelin/Dab1 and Improves Long-term Cognition in Neonatal Rats After Hypoxic-Ischemic Injury.

Publisher: Springer Country of Publication: United States NLM ID: 100929017 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-3524 (Electronic) Linking ISSN: 10298428 NLM ISO Abbreviation: Neurotox Res Subsets: MEDLINE

Publication: <2009-> : New York : Springer
Original Publication: [Amsterdam?] : Harwood Academic Publishers,

Adaptor Proteins, Signal Transducing/*antagonists & inhibitors ; Cognition/*drug effects ; Hypoxia-Ischemia, Brain/*drug therapy ; Malformations of Cortical Development, Group II/*drug therapy ; Nerve Tissue Proteins/*antagonists & inhibitors ; Reelin Protein/*antagonists & inhibitors ; Sevoflurane/*administration & dosage; Adaptor Proteins, Signal Transducing/biosynthesis ; Animals ; Animals, Newborn ; Cell Movement/drug effects ; Cell Movement/physiology ; Cognition/physiology ; Hypoxia-Ischemia, Brain/metabolism ; Hypoxia-Ischemia, Brain/pathology ; Ischemic Postconditioning/methods ; Male ; Malformations of Cortical Development, Group II/metabolism ; Malformations of Cortical Development, Group II/pathology ; Nerve Tissue Proteins/biosynthesis ; Neurons/drug effects ; Neurons/metabolism ; Neurons/pathology ; Neuroprotective Agents/administration & dosage ; Platelet Aggregation Inhibitors/administration & dosage ; Rats ; Rats, Sprague-Dawley ; Reelin Protein/biosynthesis ; Time Factors

Sevoflurane postconditioning (SPC) has been widely reported to attenuate brain injury after hypoxia-ischemia encephalopathy (HIE) by inhibiting neural necrosis and autophagy. Moreover, recent reports revealed that sevoflurane facilitated hippocampal reconstruction via regulating migration. Yet, it remains unclear whether the promotion of neural migration by SPC repairs the hippocampal injury after HIE. Here, we hypothesize that SPC exerts a neuroprotective effect by ameliorating neuronal migration disorder after HIE and regulating Reelin expression. Furthermore, the downstream Reelin/Dab1 pathway may be involved. The classical Rice-Vannucci model of hypoxia-ischemia was performed on postnatal day 7 rat pups, which was followed by SPC at 1 minimum alveolar concentration (MAC 2.5%) for 30 min. Piceatannol, causing Reelin aggregation in vivo, was used to detect whether Reelin/Dab1 was involved in the neuroprotection effect of SPC. Hippocampal-dependent learning ability tests were conducted to assess the long-term effects on locomotor activity and spatial learning ability. Our findings suggest that hypoxia-ischemia injury inhibited neurons migrated outward from the basal zone of dentate gyrus, disrupted cytoarchitecture of the dentate gyrus (DG), and led to long-term cognition deficits. However, SPC could relieve the restricted hippocampal neurons and repair the hippocampal-dependent memory function damaged after HIE by attenuating the overactivation of the Reelin/Dab1 pathway. These results demonstrate that SPC plays a pivotal role in ameliorating neuronal migration disorder and maintaining normal cytoarchitecture of the DG via inhibiting overactivated Reelin expression. This process may involve overactivated Reelin/Dab1 signaling pathway and spatial learning ability by regulating the Reelin expression which may associate with its neuroprotection.
(© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)

36th International Symposium on Intensive Care and Emergency Medicine (2016) Brussels, Belgium. 15–18 March 2016 Critical care (London, England) 20:94.  https://doi.org/10.1186/s13054-016-1208-6.
Abrous DN, Wojtowicz JM (2015) Interaction between neurogenesis and hippocampal memory system: New Vistas Cold Spring Harbor perspectives in biology 7.  https://doi.org/10.1101/cshperspect.a018952.
Barkhuizen M, van den Hove DL, Vles JS, Steinbusch HW, Kramer BW, Gavilanes AW (2017) 25 years of research on global asphyxia in the immature rat brain. Neurosci Biobehav Rev 75:166–182.  https://doi.org/10.1016/j.neubiorev.2017.01.042.
Bartley J, Soltau T, Wimborne H, Kim S, Martin-Studdard A et al (2005) BrdU-positive cells in the neonatal mouse hippocampus following hypoxic-ischemic brain injury. BMC Neurosci 6:15. https://doi.org/10.1186/1471-2202-6-15. (PMID: 10.1186/1471-2202-6-1515743533555560)
Bingham B, Liu D, Wood A, Cho S (2005) Ischemia-stimulated neurogenesis is regulated by proliferation, migration, differentiation and caspase activation of hippocampal precursor cells. Brain Res 1058:167–177.  https://doi.org/10.1016/j.brainres.2005.07.075.
Bock HH, May P (2016) Canonical and Non-Canonical Reelin Signaling Front Cell Neurosci 10:166. https://doi.org/10.3389/fncel.2016.00166. (PMID: 10.3389/fncel.2016.0016627445693)
Bruel-Jungerman E, Laroche S, Rampon C (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21:513–521. https://doi.org/10.1111/j.1460-9568.2005.03875.x. (PMID: 10.1111/j.1460-9568.2005.03875.x15673450)
Caffrey JR, Hughes BD, Britto JM, Landman KA (2014) An in Silico Agent-Based Model Demonstrates Reelin Function in Directing Lamination of Neurons during Cortical Development PloS One 9:e110415. https://doi.org/10.1371/journal.pone.0110415. (PMID: 10.1371/journal.pone.0110415)
Chai X, Frotscher M (2016) How does Reelin signaling regulate the neuronal cytoskeleton during migration? Neurogenesis (austin, Tex) 3:e1242455. https://doi.org/10.1080/23262133.2016.1242455. (PMID: 10.1080/23262133.2016.1242455)
Chai X, Forster E, Zhao S, Bock HH, Frotscher M (2009) Reelin Acts as a Stop Signal for Radially Migrating Neurons by Inducing Phosphorylation of n-Cofilin at the Leading Edge Commun Integr Biol 2:375–377.
Chen C, Shen FY, Zhao X, Zhou T, Xu DJ, Wang ZR, Wang YW (2015) Low-dose sevoflurane promotes hippocampal neurogenesis and facilitates the development of dentate gyrus-dependent learning in neonatal rats ASN Neuro 7.  https://doi.org/10.1177/1759091415575845.
Chen X, Zhou X, Yang L, Miao X, Lu DH et al (2018) Neonatal exposure to low-dose (1.2%) sevoflurane increases rats' hippocampal neurogenesis and synaptic plasticity in later life. Neurotox Res 34:188–197.  https://doi.org/10.1007/s12640-018-9877-3.
D’Arcangelo G (2005) The reeler mouse: anatomy of a mutant. Int Rev Neurobiol 71:383–417. https://doi.org/10.1016/s0074-7742(05)71016-3. (PMID: 10.1016/s0074-7742(05)71016-316512359)
De Rubeis S, He X, Goldberg AP, Poultney CS, Samocha K et al (2014) Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515:209–215.  https://doi.org/10.1038/nature13772.
Folsom TD, Fatemi SH (2013) The involvement of Reelin in neurodevelopmental disorders. Neuropharmacology 68:122–135. https://doi.org/10.1016/j.neuropharm.2012.08.015. (PMID: 10.1016/j.neuropharm.2012.08.01522981949)
Frotscher M, Haas CA, Forster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640. (PMID: 10.1093/cercor/13.6.634)
Gilbert PE, Kesner RP, Lee I (2001) Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1 Hippocampus 11:626–636.  https://doi.org/10.1002/hipo.1077.
Golan MH, Mane R, Molczadzki G, Zuckerman M, Kaplan-Louson V, Huleihel M, Perez-Polo JR (2009) Impaired migration signaling in the hippocampus following prenatal hypoxia. Neuropharmacology 57:511–522. https://doi.org/10.1016/j.neuropharm.2009.07.028. (PMID: 10.1016/j.neuropharm.2009.07.02819635490)
Gonzalez-Billault C, Del Rio JA, Urena JM, Jimenez-Mateos EM, Barallobre MJ et al (2005) A role of MAP1B in Reelin-dependent neuronal migration Cereb Cortex 15:1134–1145.  https://doi.org/10.1093/cercor/bhh213.
Gustavsson M, Anderson MF, Mallard C, Hagberg H (2005) Hypoxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr Res 57:305–309. https://doi.org/10.1203/01.pdr.0000151122.58665.70. (PMID: 10.1203/01.pdr.0000151122.58665.7015611346)
Hack I, Bancila M, Loulier K, Carroll P, Cremer H (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci 5:939–945. https://doi.org/10.1038/nn923. (PMID: 10.1038/nn92312244323)
He M, Zhang ZH, Guan CB, Xia D, Yuan XB (2010) Leading tip drives soma translocation via forward F-actin flow during neuronal migration. J Neurosci 30:10885–10898. https://doi.org/10.1523/JNEUROSCI.0240-10.2010. (PMID: 10.1523/JNEUROSCI.0240-10.2010207027176634710)
Hevner RF (2016) Evolution of the mammalian dentate gyrus. J Comp Neurol 524:578–594. https://doi.org/10.1002/cne.23851. (PMID: 10.1002/cne.2385126179319)
Huang YY, Li L, Monteleone M, Ferrari L, States LJ et al (2016) Use of anesthesia for imaging studies and interventional procedures in children. J Neurosurg Anesthesiol 28:400–404. https://doi.org/10.1097/ana.0000000000000355. (PMID: 10.1097/ana.000000000000035527564559)
Kerjan G, Gleeson JG (2007) Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly Trends in genetics. TIG 23:623–630. https://doi.org/10.1016/j.tig.2007.09.003. (PMID: 10.1016/j.tig.2007.09.00317997185)
Knuesel I (2010) Reelin-mediated signaling in neuropsychiatric and neurodegenerative diseases. Prog Neurobiol 91:257–274. https://doi.org/10.1016/j.pneurobio.2010.04.002. (PMID: 10.1016/j.pneurobio.2010.04.00220417248)
Kohno S, Kohno T, Nakano Y, Suzuki K, Ishii M et al (2009) Mechanism and significance of specific proteolytic cleavage of Reelin. Biochem Biophys Res Commun 380:93–97. https://doi.org/10.1016/j.bbrc.2009.01.039. (PMID: 10.1016/j.bbrc.2009.01.03919166810)
Kohno T (2017) Regulatory mechanisms and physiological significance of Reelin function Yakugaku zasshi. J Pharm Soc Jpn 137:1233–1240. https://doi.org/10.1248/yakushi.17-00127. (PMID: 10.1248/yakushi.17-00127)
Komitova M, Xenos D, Salmaso N, Tran KM, Brand T et al (2013) Hypoxia-induced developmental delays of inhibitory interneurons are reversed by environmental enrichment in the postnatal mouse forebrain. J Neurosci 33:13375–13387. https://doi.org/10.1523/JNEUROSCI.5286-12.2013. (PMID: 10.1523/JNEUROSCI.5286-12.2013239463953742925)
Kubo K, Mikoshiba K, Nakajima K (2002) Secreted Reelin Molecules Form Homodimers Neurosci Res 43:381–388. (PMID: 12135781)
Lai Z, Zhang L, Su J, Cai D, Xu Q (2016) Sevoflurane postconditioning improves long-term learning and memory of neonatal hypoxia-ischemia brain damage rats via the PI3K/Akt-mPTP pathway. Brain Res 1630:25–37.  https://doi.org/10.1016/j.brainres.2015.10.050.
Lauer-Fields JL, Spicer TP, Chase PS, Cudic M, Burstein GD et al (2008) Screening of potential a disintegrin and metalloproteinase with thrombospondin motifs-4 inhibitors using a collagen model fluorescence resonance energy transfer substrate. Anal Biochem 373:43–51.  https://doi.org/10.1016/j.ab.2007.09.014.
Lepousez G, Nissant A, Lledo PM (2015) Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86:387–401. https://doi.org/10.1016/j.neuron.2015.01.002. (PMID: 10.1016/j.neuron.2015.01.00225905812)
Levy AD, Omar MH, Koleske AJ (2014) Extracellular matrix control of dendritic spine and synapse structure and plasticity in adulthood. Front Neuroanat 8:116. https://doi.org/10.3389/fnana.2014.00116. (PMID: 10.3389/fnana.2014.00116253685564202714)
Li L, Saiyin H, Xie J, Ma L, Xue L et al (2017) Sevoflurane preconditioning induced endogenous neurogenesis against ischemic brain injury by promoting microglial activation oncotarget 8:28544–28557. https://doi.org/10.18632/oncotarget.15325. (PMID: 10.18632/oncotarget.1532528212538)
Li Y, Gonzalez P, Zhang L (2012) Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions. Prog Neurobiol 98:145–165. https://doi.org/10.1016/j.pneurobio.2012.05.010. (PMID: 10.1016/j.pneurobio.2012.05.010226274923404248)
Liu F, Shi J, Tanimukai H, Gu J, Gu J et al (2009) Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer’s disease. Brain : a Journal of Neurology 132:1820–1832. https://doi.org/10.1093/brain/awp099. (PMID: 10.1093/brain/awp099)
Ma Q, Dasgupta C, Li Y, Huang L, Zhang L (2019) MicroRNA-210 Downregulates ISCU and induces mitochondrial dysfunction and neuronal death in neonatal hypoxic-ischemic brain injury. Mol Neurobiol 56(8):5608-5625.  https://doi.org/10.1007/s12035-019-1491-8.
Ma Q, Zhang L (2015) Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia. Prog Neurobiol 124:28–48. https://doi.org/10.1016/j.pneurobio.2014.11.001. (PMID: 10.1016/j.pneurobio.2014.11.00125450949)
Meseke M, Cavus E, Förster E (2013) Reelin promotes microtubule dynamics in processes of developing neurons. Histochem Cell Biol 139:283–297. https://doi.org/10.1007/s00418-012-1025-1. (PMID: 10.1007/s00418-012-1025-122990595)
Millar LJ, Shi L, Hoerder-Suabedissen A, Molnar Z (2017) Neonatal hypoxia ischaemia: mechanisms, models, and therapeutic challenges. Front Cell Neurosci 11:78.  https://doi.org/10.3389/fncel.2017.00078.
Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250. https://doi.org/10.1146/annurev.neuro.28.051804.101459. (PMID: 10.1146/annurev.neuro.28.051804.101459)
Moskowitz MA, Lo EH, Iadecola C (2010) The science of stroke: mechanisms in search of treatments. Neuron 67:181–198. https://doi.org/10.1016/j.neuron.2010.07.002. (PMID: 10.1016/j.neuron.2010.07.002206708282957363)
Nichols AJ, Olson EC (2010) Reelin promotes neuronal orientation and dendritogenesis during preplate splitting. Cereb Cortex 20:2213–2223. https://doi.org/10.1093/cercor/bhp303. (PMID: 10.1093/cercor/bhp303200649402950812)
Ogden KK, Ozkan ED, Rumbaugh G (2016) Prioritizing the development of mouse models for childhood brain disorders. Neuropharmacology 100:2–16. https://doi.org/10.1016/j.neuropharm.2015.07.029. (PMID: 10.1016/j.neuropharm.2015.07.02926231830)
Pan YW, Chan GC, Kuo CT, Storm DR, Xia Z (2012) Inhibition of adult neurogenesis by inducible and targeted deletion of ERK5 mitogen-activated protein kinase specifically in adult neurogenic regions impairs contextual fear extinction and remote fear memory. J Neurosci 32:6444–6455.  https://doi.org/10.1523/JNEUROSCI.6076-11.2012.
Piatti VC, Esposito MS, Schinder AF (2006) The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist 12:463–468. https://doi.org/10.1177/1073858406293538. (PMID: 10.1177/107385840629353817079512)
Pocock R, Hobert O (2008) Oxygen levels affect axon guidance and neuronal migration in Caenorhabditis elegans. Nat Neurosci 11:894–900. https://doi.org/10.1038/nn.2152. (PMID: 10.1038/nn.215218587389)
Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM et al (2010) Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci 30:4636–4649. https://doi.org/10.1523/JNEUROSCI.5284-09.2010. (PMID: 10.1523/JNEUROSCI.5284-09.2010203571146632327)
Ren X, Wang Z, Ma H, Zuo Z (2014) Sevoflurane postconditioning provides neuroprotection against brain hypoxia-ischemia in neonatal rats. Neurol Sci 35:1401–1404. https://doi.org/10.1007/s10072-014-1726-4. (PMID: 10.1007/s10072-014-1726-424705859)
Sebastian V, Diallo A, Ling DS, Serrano PA (2013) Robust training attenuates TBI-induced deficits in reference and working memory on the radial 8-arm maze. Front Behav Neurosci 7:38.  https://doi.org/10.3389/fnbeh.2013.00038.
Song B, Ao Q, Wang Z, Liu W, Niu Y et al (2013) Phosphorylation of Tau Protein over Time in Rats Subjected to Transient Brain Ischemia Neural Regeneration Research 8:3173–3182. https://doi.org/10.3969/j.issn.1673-5374.2013.34.001. (PMID: 10.3969/j.issn.1673-5374.2013.34.00125206638)
Umeshima H, Hirano T, Kengaku M (2007) Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc Natl Acad Sci USA 104:16182–16187. https://doi.org/10.1073/pnas.0708047104. (PMID: 10.1073/pnas.0708047104179138732000450)
Wang S, Xue H, Xu Y, Niu J, Zhao P (2018) Sevoflurane postconditioning inhibits autophagy through activation of the extracellular signal-regulated kinase cascade, alleviating hypoxic-ischemic brain injury in neonatal rats. Neurochem Res 44(2):347–356.  https://doi.org/10.1007/s11064-018-2682-9.
Wang Z, Ye Z, Huang G, Wang N, Wang E, Guo Q (2016) Sevoflurane post-conditioning enhanced hippocampal neuron resistance to global cerebral ischemia induced by cardiac arrest in rats through PI3K/Akt survival pathway. Front Cell Neurosci 10:271.  https://doi.org/10.3389/fncel.2016.00271.
Warner DO, Zaccariello MJ, Katusic SK, Schroeder DR, Hanson AC et al (2018) Neuropsychological and behavioral outcomes after exposure of young children to procedures requiring general anesthesia: the mayo anesthesia safety in kids (MASK) study anesthesiology 129:89–105.  https://doi.org/10.1097/aln.0000000000002232.
Wen J, Lin H, Zhao M, Tao L, Yang Y et al (2018) Piceatannol attenuates D-GalN/LPS-induced hepatoxicity in mice: involvement of ER stress, inflammation and oxidative stress. Int Immunol 64:131–139.  https://doi.org/10.1016/j.intimp.2018.08.037.
Xu Y, Tian Y, Tian Y, Li X, Zhao P (2016) Autophagy activation involved in hypoxic-ischemic brain injury induces cognitive and memory impairment in neonatal rats. J Neurochem 139:795–805. https://doi.org/10.1111/jnc.13851. (PMID: 10.1111/jnc.1385127659442)
Xue H, Xu Y, Wang S, Wu ZY, Li XY et al (2019) Sevoflurane post-conditioning alleviates neonatal rat hypoxic-ischemic cerebral injury via Ezh2-regulated autophagy. Drug Des Devel Ther 13:1691–1706.  https://doi.org/10.2147/DDDT.S197325.
Yang Q, Yan W, Li X, Hou L, Dong H et al (2012) Activation of canonical notch signaling pathway is involved in the ischemic tolerance induced by sevoflurane preconditioning in mice. Anesthesiology 117:996–1005. https://doi.org/10.1097/ALN.0b013e31826cb469. (PMID: 10.1097/ALN.0b013e31826cb46922929735)
Yu Q, Li L, Liang WM (2019) Effect of sevoflurane preconditioning on astrocytic dynamics and neural network formation after cerebral ischemia and reperfusion in rats neural regeneration research 14:265–271. https://doi.org/10.4103/1673-5374.244790. (PMID: 10.4103/1673-5374.24479030531009)
Zhao H, Mitchell S, Koumpa S, Cui YT, Lian Q et al (2016) Heme oxygenase-1 mediates neuroprotection conferred by argon in combination with hypothermia in neonatal hypoxia-ischemia brain injury. Anesthesiology 125:180–192.  https://doi.org/10.1097/ALN.0000000000001128.
Zhao P, Ji G, Xue H, Yu W, Zhao X et al (2014) Isoflurane postconditioning improved long-term neurological outcome possibly via inhibiting the mitochondrial permeability transition pore in neonatal rats after brain hypoxia-ischemia. Neuroscience 280:193–203. https://doi.org/10.1016/j.neuroscience.2014.09.006. (PMID: 10.1016/j.neuroscience.2014.09.00625241064)
Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells Development (Cambridge, England) 131:5117–5125.  https://doi.org/10.1242/dev.01387.
Zhang Y, Zhang LH, Chen X, Zhang N, Li G (2018) Piceatannol attenuates behavioral disorder and neurological deficits in aging mice via activating the Nrf2 pathway. Food Funct 9:371–378.  https://doi.org/10.1039/c7fo01511a.

No.82071215 Natural Science Foundation of Liaoning Province; No.81870838 Natural Science Foundation of Liaoning Province; No.2018225004 Key Research and Development Program of Liaoning Province; No. 201708 Outstanding Scientific Fund of Shengjing Hospital; No.19-110-4-24,No.20-204-4-44 Shenyang Clinical medicine Research Center of Anesthesiology

Keywords: Hippocampal dentate gyrus; Hypoxia–ischemia; Long-term neurocognition; Reelin; Sevoflurane postconditioning

0 (Adaptor Proteins, Signal Transducing)
0 (Dab1 protein, rat)
0 (Nerve Tissue Proteins)
0 (Neuroprotective Agents)
0 (Platelet Aggregation Inhibitors)
0 (Reelin Protein)
0 (Reln protein, rat)
38LVP0K73A (Sevoflurane)

Date Created: 20210705 Date Completed: 20220202 Latest Revision: 20220202

20231215

10.1007/s12640-021-00377-3

34224102