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Postconditioning with Sevoflurane or Propofol Alleviates Lipopolysaccharide-Induced Neuroinflammation but Exerts Dissimilar Effects on the NR2B Subunit and Cognition

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Abstract

Neuroinflammation can cause cognitive deficits, and preexisting neuroinflammation is observed frequently in the clinic after trauma, surgery, and infection. Patients with preexisting neuroinflammation often need further medical treatment under general anesthesia. However, the effects of postconditioning with general anesthetics on preexisting neuroinflammation have not been determined. In this study, adult rats were posttreated with sevoflurane or propofol after intracerebroventricular administration of lipopolysaccharide. The effects of sevoflurane or propofol postconditioning on neuroinflammation-induced recognition memory deficits were detected. Our results found that postconditioning with sevoflurane but not propofol reversed the selective spatial recognition memory impairment induced by neuroinflammation, and these differential effects did not appear to be associated with the similar anti-neuroinflammatory responses of general anesthetics. However, postconditioning with propofol induced a selective long-lasting upregulation of extrasynaptic NR2B-containing N-methyl-D-aspartate receptors in the dorsal hippocampus, which downregulated the cAMP response element-binding signaling pathway and impaired spatial recognition memory. Additionally, the NR2B antagonists memantine and Ro25-6981 reversed this neurotoxicity induced by propofol postconditioning. Taken together, these results indicate that under preexisting neuroinflammation, postconditioning with sevoflurane can provide reliable neuroprotection by attenuating lipopolysaccharide-induced neuroinflammation, apoptosis, and neuronal loss and eventually improving spatial recognition deficits. However, although posttreatment with propofol also has the same anti-neuroinflammatory effects, the neurotoxicity caused by propofol postconditioning following neuroinflammation warrants further consideration.

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Data Availability

The data used during the present study are available from the corresponding author upon reasonable request.

References

  1. Kitano H, Kirsch JR, Hurn PD, Murphy SJ (2007) Inhalational anaesthetics as neuroprotectants or chemical1preconditioning agents in ischemic brain. J Cereb Blood Flow Metab 27(6):1108–1128. https://doi.org/10.1038/sj.jcbfm.9600410

    Article  CAS  PubMed  Google Scholar 

  2. Wang J-K, Yu L-N, Zhang F-J, Yang M-J, Yu J, Yan M et al (2010) Postconditioning with sevoflurane protects against focal cerebral ischemia and reperfusion injury via PI3K/Akt pathway. Brain Res 1357:142–151. https://doi.org/10.1016/j.brainres.2010.08.009

    Article  CAS  PubMed  Google Scholar 

  3. Hwang J-W, Jeon Y-T, Lim Y-J, Park H-P (2017) Sevoflurane postconditioning-induced anti-inflammation via inhibition of the toll-like receptor-4/nuclear factor kappa B pathway contributes to neuroprotection against transient global cerebral ischemia in rats. Int J Mol Sci 18(11):2347. https://doi.org/10.3390/ijms18112347

    Article  CAS  PubMed Central  Google Scholar 

  4. Wang H, Wang G, Yu Y, Wang Y (2009) The role of phosphoinositide-3-kinase/Akt pathway in4. propofol-induced postconditioning against focal cerebral ischemia-reperfusion injury in rats. Brain Res 1297:177–184. https://doi.org/10.1016/j.brainres.2009.08.054

    Article  CAS  PubMed  Google Scholar 

  5. Liang C, Cang J, Wang H, Xue Z (2013) Propofol attenuates cerebral ischemia/reperfusion injury partially using heme oxygenase-1. J Neurosurg Anesthesiol 25(3):311–316. https://doi.org/10.1097/ANA.0b013e31828c6af5

    Article  CAS  PubMed  Google Scholar 

  6. Huang C, Ng OT-W, Chu JM-T, Irwin MG, Hu X, Zhu S et al (2019) Differential effects of propofol and6. dexmedetomidine on neuroinflammation induced by systemic endotoxin lipopolysaccharides in adult mice. Neurosci Lett 707:134309. https://doi.org/10.1016/j.neulet.2019.134309

    Article  CAS  PubMed  Google Scholar 

  7. Ye X, Lian Q, Eckenhoff MF, Eckenhoff RG, Pan JZ (2013) Differential general anesthetic effects on microglial cyktokine expression. PLoS One 8(1):e52887. https://doi.org/10.1371/journal.pone.0052887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Shaw K, Commins S, O’Mara SM (2001) Lipopolysaccharide causes deficits in spatial learning in the water maze but not in BDNF expression in the rat dentate gyrus. Behav Brain Res 124(1):47–54. https://doi.org/10.1016/s0166-4328(01)00232-7

    Article  CAS  PubMed  Google Scholar 

  9. Sparkman NL, Kohman RA, Scott VJ, Boehm GW (2005) Bacterial endotoxin-induced behavioral alterations in two variations of the Morris water maze. Physiol Behav 86(1-2):244–251. https://doi.org/10.1016/j.physbeh.2005.07.016

    Article  CAS  PubMed  Google Scholar 

  10. Irifune M, Takarada T, Shimizu Y, Endo C, Katayama S, Dohi T et al (2003) Propofol-induced anaesthesia in mice is mediated by gamma-aminobutyric acid-A and excitatory amino acid receptors. Anesth Analg 97(2):424–429. https://doi.org/10.1213/01.ane.0000059742.62646.40

    Article  CAS  PubMed  Google Scholar 

  11. Kelly EW, Solt K, Raines DE (2007) Volatile aromatic anaesthetics variably impact gamma-aminobutyric acid type A receptor function. Anesth Analg 105(5):1287–1292. https://doi.org/10.1213/01.ane.0000282829.21797.97

    Article  CAS  PubMed  Google Scholar 

  12. Newcomer JW, Krystal JH (2001) NMDA receptor regulation of memory and behavior in humans. Hippocampus 11(5):529–542. https://doi.org/10.1002/hipo.1069

    Article  CAS  PubMed  Google Scholar 

  13. Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptor. Nature 438(7065):185–192. https://doi.org/10.1038/nature04089

    Article  CAS  PubMed  Google Scholar 

  14. Rammes G, Starker LK, Haseneder R, Berkmann J, Alexandra P, Zieglgänsberger W (2009) Isoflurane anaesthesia reversibly improve cognitive function and long-term potentiation (LTP) via an up-regulation in NMDA receptor 2B subunit expression. Neuropharmacology 56(3):626–636. https://doi.org/10.1016/j.neuropharm.2008.11.002

    Article  CAS  PubMed  Google Scholar 

  15. Monaco SA, Gulchina Y, Gao W-J (2015) NR2B subunit in the prefrontal cortex: A double-edged sword for working memory function and psychiatric disorders. Neurosci Biobehav Rev 56:127–138. https://doi.org/10.1016/j.neubiorev.2015.06.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Liu J, Zhang X, Zhang W, Gu G, Wang P (2015) Effects of sevoflurane on young male adult C57BL/6 mice spatial cognition. PLoS One 10(8):e0134217. https://doi.org/10.1371/journal.pone.0134217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang Y, Han S, Han R, Su Y, Li J (2017) Propofol-induced downregulation of NR2B membrane translacation in hippocampus and spatial memory deficits of neonatal mice. Brain Behav 7(7):e00734. https://doi.org/10.1002/brb3.734

    Article  PubMed  PubMed Central  Google Scholar 

  18. Okamoto S, Pouladi MA, Talantova M, Yao D, Xia P, Ehrnhoefer DE et al (2009) Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15(12):1407–1413. https://doi.org/10.1038/nm.2056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011) Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 31(18):6627–6638. https://doi.org/10.1523/JNEUROSCI.0203-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11(10):682–696. https://doi.org/10.1038/nrn.2911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5(5):405–414. https://doi.org/10.1038/nn835

    Article  CAS  PubMed  Google Scholar 

  22. Gouix E, Léveillé F, Nicole O, Melon C, Had-Aissouni L, Buisson A (2009) Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation. Mol Cell Neurosci 40(4):463–473. https://doi.org/10.1016/j.mcn.2009.01.002

    Article  CAS  PubMed  Google Scholar 

  23. Wang W-Y, Jia L-J, Luo Y, Zhang H-H, Cai F, Mao H et al (2016) Location- and subunit-specific NMDA receptors determine the developmental sevoflurane neurotoxicity through ERK1/2 signaling. Mol Neurobiol 53(1):216–230. https://doi.org/10.1007/s12035-014-9005-1

    Article  CAS  PubMed  Google Scholar 

  24. Li L, Li Z, Cao Y, Fan D, Chui D, Guo X (2016) Increased extrasynaptic GluN2B expression is involved in cognitive impairment after isoflurane anesthesia. Exp Ther Med 12(1):161–168. https://doi.org/10.3892/etm.2016.3306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gong Q-H, Wang Q, Pan L-L, Liu X-H, Huang H, Zhu Y-Z (2010) Hydrogen sulfide attenuates lipopolysaccharide-induecd cognitive impairment: a proinflammatory pathway in rats. Pharmacol Biochem Behav 96(1):52–58. https://doi.org/10.1016/j.pbb.2010.04.006

    Article  CAS  PubMed  Google Scholar 

  26. Vedder LC, Smith CC, Flannigan AE, McMahon LL (2013) Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors. Hippocampus 23(1):108–115. https://doi.org/10.1002/hipo.22068

    Article  CAS  PubMed  Google Scholar 

  27. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Elesvier

  28. Jiang CH, Lee S, Park IY, Song A, Moon C, Cho GW (2019) Memantine attenuates salicylate-induced tinnitus possibly by reducing NR2B expression in auditory cortex of rat. Exp Neurobiol 28(4):495–503. https://doi.org/10.5607/en.2019.28.4.495

    Article  Google Scholar 

  29. Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31(29):10721–10731. https://doi.org/10.1523/JNEUROSCI.6413-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chen B, Deng X, Wang B, Liu H (2016) Etanercept, an inhibitor of TNF-α, prevents propofol-induced neurotoxicity in the developing brain. Int J Dev Neurosci 55:91–100. https://doi.org/10.1016/j.ijdevneu.2016.10.002

    Article  CAS  PubMed  Google Scholar 

  31. Chen B, Deng X, Wang B, Liu H (2016) Persistent neuronal apoptosis and synaptic loss induced by multiple but not single exposure of propofol contribute to long-term cognitive dysfunction in neonatal rats. J Toxicol Sci 41(5):627–636. https://doi.org/10.2131/jts.41.627

    Article  CAS  PubMed  Google Scholar 

  32. Zhang Z, Song Z, Shen F, Xie P, Wang J, Zhu A, Zhu G (2020) Ginsenoside Rg1 prevents PTSD-like behaviors in mice through promoting synaptic proteins, reducing Kir4.1 and TNF-α in the hippocampus. Mol Neurobiol. https://doi.org/10.1007/s12035-020-02213-9

  33. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin-I (Protein-I), a nerve terminal-specific phosphoprotein .III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96(5):1374–1388. https://doi.org/10.1083/jcb.96.5.1374

    Article  CAS  PubMed  Google Scholar 

  34. Carlin RK, Grab DJ, Cohen RS, Siekevitz P (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86(3):831–845. https://doi.org/10.1083/jcb.86.3.831

    Article  CAS  PubMed  Google Scholar 

  35. Smith KE, Gibson ES, Dell’Acqua ML (2006) cAMP-dependent protein kinase postsynaptic localization regulated by NMDA receptor activation through translocation of an A-kinase anchoring protein scaffold protein. J Neurosci 26(9):2391–2402. https://doi.org/10.1523/JNEUROSCI.3092-05.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Matus AI, Taff-Jones DH (1978) Morphology and molecular composition of isolated postsynaptic junctional structures. Proc R Soc Lond B Biol Sci 203(1151):135–151. https://doi.org/10.1098/rspb.1978.0097

    Article  CAS  PubMed  Google Scholar 

  37. Philips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W et al (2001) The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32(1):63–77. https://doi.org/10.1016/s0896-6273(01)00450-0

    Article  Google Scholar 

  38. Milnerwood AJ, Gladding CM, Pouladi MA, Kaufman AM, Hines RM, Boyd JD et al (2010) Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington’s disease mice. Neuron 65(2):178–190. https://doi.org/10.1016/j.neuron.2010.01.008

    Article  CAS  PubMed  Google Scholar 

  39. Deng X, Chen B, Wang B, Zhang J, Liu H (2017) TNF-α mediates the intrinsic and extrinsic pathway in propofol-induced neuronal apoptosis via PI3K/Akt signaling pathway in rat prefrontal cortical neurons. Neurotox Res 32(3):409–419. https://doi.org/10.1007/s12640-017-9751-8

    Article  CAS  PubMed  Google Scholar 

  40. Shi D-D, Huang Y-H, Lai CSW, Dong CM, Ho LC, Li X-Y et al (2019) Ginsenoside Rg1 prevents chemotherapy-induced cognitive impairment: associations with microglia-mediated cytokines, neuroinflammation, and neuroplasticity. Mol Neurobiol 56:5626–5642. https://doi.org/10.1007/s12035-019-1474-9

    Article  CAS  PubMed  Google Scholar 

  41. Zarifkar A, Choopani S, Ghasemi R, Naghdi N, Maghsoudi AH, Maghsoudi N et al (2010) Agmatine prevents LPS-induced spatial memory impairment and hippocampal apoptosis. Eur J Pharmacol 634(1-3):84–88. https://doi.org/10.1016/j.ejphar.2010.02.029

    Article  CAS  PubMed  Google Scholar 

  42. Feng Y, Xue H, Zhu J, Yang L, Zhang F, Qian R et al (2016) ESE1 is associated with neuronal apoptosis in lipopolysaccharide induced neuroinflammation. Neurochem Res 41(10):2752–2762. https://doi.org/10.1007/s11064-016-1990-1

    Article  CAS  PubMed  Google Scholar 

  43. Wang K-C, Fan L-W, Kaizaki A, Pang Y, Cai Z, Tien L-T (2013) Neonatal lipopolysaccharide exposure induces long-lasting learning impairment, less anxiety-like response and hippocampal injury in adult rats. Neuroscience 234:146–157. https://doi.org/10.1016/j.neuroscience.2012.12.049

    Article  CAS  PubMed  Google Scholar 

  44. Lu W, Roche KW (2012) Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol 22(3):470–479. https://doi.org/10.1016/j.conb.2011.09.008

    Article  CAS  PubMed  Google Scholar 

  45. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12(3):529–540. https://doi.org/10.1016/0896-6273(94)90210-0

    Article  CAS  PubMed  Google Scholar 

  46. Parsons MP, Raymond LA (2014) Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82(2):279–293. https://doi.org/10.1016/j.neuron.2014.03.030

    Article  CAS  PubMed  Google Scholar 

  47. Varbanov H, Dityatev A (2017) Regulation of extrasynaptic signaling by polysialylated NCAM: impact for synaptic plasticity and cognitive function. Mol Cell Neurosci 81:12–21. https://doi.org/10.1016/j.mcn.2016.11.005

    Article  CAS  PubMed  Google Scholar 

  48. Goebel-Goody SM, Davies KD, Alvestad Linger RM, Freund RK, Browning MD (2009) Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices. Neuroscience 158(4):1446–1459. https://doi.org/10.1016/j.neuroscience.2008.11.006

    Article  CAS  PubMed  Google Scholar 

  49. Stazi M, Wirths O (2021) Chronic memantine treatment ameliorates behavioral deficits, neuron loss, and impaired neurogenesis in a model of Alzheimer’s disease. Mol Neurobiol 58(1):204–216. https://doi.org/10.1007/s12035-020-02120-z

    Article  PubMed  Google Scholar 

  50. Fisher G, Mutel V, Trube G, Malherbe P, Kew JN, Mohasci E et al (1997) Ro25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 283(3):1285–1292

    Google Scholar 

  51. Zarbato GF, de Souza Goldim MP, Giustina AD, Danielski LG, Mathias K, Florentino D et al (2018) Dimethyl fumarate limits neuroinflammation and oxidative stress and improves cognitive impairment after polymicrobial sepsis. Neurotox Res 34(3):418–430. https://doi.org/10.1007/s12640-018-9900-8

    Article  CAS  PubMed  Google Scholar 

  52. Safavynia SA, Goldstein PA (2019) The role of neuroinflammation in postoperative cognitive dysfunction: moving from hypothesis to treatment. Front Psychiatry 9:752. https://doi.org/10.3389/fpsyt.2018.00752

    Article  PubMed  PubMed Central  Google Scholar 

  53. Tripathi A, Paliwal P, Krishnamurthy S (2017) Piracetam attenuates LPS-induced neuroinflammation and cognitive impairment in rats. Cell Mol Neurobiol 37(8):1373–1386. https://doi.org/10.1007/s10571-017-0468-2

    Article  CAS  PubMed  Google Scholar 

  54. Belarbi K, Jopson T, Tweedie D, Arellano C, Luo W, Greig NH et al (2012) TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation 9:23. https://doi.org/10.1186/1742-2094-9-23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Cholvin T, Loureiro M, Cassel R, Cosquer B, Herbeaux K, de Vasconcelos AP et al (2016) Dorsal hippocampus and medial prefrontal cortex each contribute to the retrieval of a recent spatial memory in rats. Brain Struct Funct 221(1):91–102. https://doi.org/10.1007/s00429-014-0894-6

    Article  PubMed  Google Scholar 

  56. Ennaceur A, Neave N, Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80(1-2):9–25. https://doi.org/10.1016/0166-4328(96)00006-x

    Article  CAS  PubMed  Google Scholar 

  57. Hannesson DK, Vacca G, Howland JG, Phillips AG (2004) Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in cortex. Psychopharmacology 232(24):4433–4444. https://doi.org/10.1007/s00213-015-4071-2

    Article  CAS  Google Scholar 

  58. Tosaka S, Tosaka R, Matsumoto S, Maekawa T, Cho S, Sumikawa K (2011) Roles of cyclooxygenase 2 in sevoflurane- and olprinone-induced early phase of preconditioning and postconditioning against myocardial infarction in rat hearts. J Cardiovasc Pharmacol Ther 16(1):72–78. https://doi.org/10.1177/1074248410380208

    Article  CAS  PubMed  Google Scholar 

  59. Hu X, Wang J, Zhang Q, Duan X, Chen Z, Zhang Y (2016) Postconditioning with sevoflurane amileorates spatial learning and memory deficit after hemorrhage shock and resuscitation in rats. J Surg Res 206(2):307–315. https://doi.org/10.1016/j.jss.2016.08.026

    Article  CAS  PubMed  Google Scholar 

  60. Luo C, Zhang YL, Luo W, Zhou FH, Li CQ, Xu JM, et al (2015) Differential effects of general anesthetics on anxiety-like behavior in formalin-induced pain: involvement of ERK activation in the anterior cingulate

  61. Schoen J, Husemann L, Tiemeyer C, Lueloh A, Sedemund-Adib B, Berger KU et al (2011) Cognitive function after sevoflurane- vs propofol-based anaesthesia for on-pump cardiac surgery: a randomized controlled trial. Br J Anaesth 106(6):840–850. https://doi.org/10.1093/bja/aer091

    Article  CAS  PubMed  Google Scholar 

  62. Hardingham GE, Bading H (2003) The yin and yang of NMDA receptor signalling. Trends Neurosci 26(2):81–89. https://doi.org/10.1016/S0166-2236(02)00040-1

    Article  CAS  PubMed  Google Scholar 

  63. Warburton EC, Barker GR, Brown MW (2013) Investigations into the involvement of NMDA mechanisms in recognition memory. Neuropharmacology 74(100):41–47. https://doi.org/10.1016/j.neuropharm.2013.04.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Réus GZ, Valvassori SS, Machado RA, Martins MR, Gavioli EC, Quevedo J (2007) Acute treatment with low doses of memantine does not impair aversive, non-associative and recognition memory in rats. Naunyn Schmiedeberg's Arch Pharmacol 376(5):295–300. https://doi.org/10.1007/s00210-007-0235-x

    Article  CAS  Google Scholar 

  65. Danysz W, Parsons CG (2002) Neuroprotective potential of ionotropic glutamate receptor antagonists. Neurotox Res 4(2):119–126. https://doi.org/10.1080/10298420290015872

    Article  CAS  PubMed  Google Scholar 

  66. Wu Q, Zheng R, Srisai D, McKnight GS, Palmiter RD (2013) NR2B subunit of the NMDA glutamate receptor regulates appetite in the parabrachial nucleus. Proc Natl Acad Sci U S A 110(36):14765–14770. https://doi.org/10.1073/pnas.1314137110

    Article  PubMed  PubMed Central  Google Scholar 

  67. Jiang M, Zhang W, Ma Z, Gu X (2013) Antinociception and prevention of hyperalgesia by intrathecal administration of Ro 25-6981, a highly selective antagonist of the 2B subunit of N-methyl-D-aspartate receptor. Pharmacol Biochem Behav 112:56–63. https://doi.org/10.1016/j.pbb.2013.09.007

    Article  CAS  PubMed  Google Scholar 

  68. Zhan Y, Xia J, Wang X (2020) Effects of glutamate-related drugs on anxiety and compulsive behavior in rats with obsessive-compulsive disorder. Int J Neurosci 130(6):551–560. https://doi.org/10.1080/00207454.2019.1684276

    Article  CAS  PubMed  Google Scholar 

  69. Chen Y, Chen A, Luo X, Guo L, Tang Y, Bao C et al (2014) Hippocampal NR2B-containing NMDA receptors enhance long-term potentiation in rats with chronic visceral pain. Brain Res 1570:43–53. https://doi.org/10.1016/j.brainres.2014.05.001

    Article  CAS  PubMed  Google Scholar 

  70. Luciano-Jaramillo J, Sandoval-García F, Vázquez-Del Mercado M, Gutiérrez-Mercado YK, Navarro-Hernández RE, Martínez-García EA et al (2019) Downregulation of hippocampal NR2A/2B subunits related to cognitive impairment in a pristane-induced lupus BALB/c mice. PLoS One 14(9):e0217190. https://doi.org/10.1371/journal.pone.0217190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chen D, Qi X, Zhuang R, Cao J, Xu Y, Huang X et al (2019) Prenatal propofol exposure downregulates NMDA receptor expression and causes cognitive and emotional disorders in rats. Eur J Pharmacol 843:268–276. https://doi.org/10.1016/j.ejphar.2018.11.032

    Article  CAS  PubMed  Google Scholar 

  72. Stabernack C, Sonner JM, Laster M, Zhang Y, Xing Y, Sharma M et al (2003) Spinal N-methyl-d-aspartate receptors may contribute to the immobilizing action of isoflurane. Anesth Analg 96(1):102–107. https://doi.org/10.1097/00000539-200301000-00022

    Article  CAS  PubMed  Google Scholar 

  73. Franks NP (2006) Molecular targets underlying general anaesthesia. Br J Pharmacol 147(Suppl 1(Suppl1)):S72–S81. https://doi.org/10.1038/sj.bjp.0706441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Gladding CM, Raymond LA (2011) Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci 48(4):308–320. https://doi.org/10.1016/j.mcn.2011.05.001

    Article  CAS  PubMed  Google Scholar 

  75. Wang WY, Luo Y, Jia LJ, Hu SF, Lou XK, Shen SL et al (2014) Inhibition of aberrant cyclin-dependent kinase 5 activity attenuates isoflurane neurotoxicity in the developing brain. Neuropharmacology 77:90–99. https://doi.org/10.1016/j.neuropharm.2013.09.006

    Article  CAS  PubMed  Google Scholar 

  76. Yang X, Zhang W, Wu H, Fu S, Yang J, Liu S et al (2020) Downregulation of CDK5 restores sevoflurane-induced cognitive dysfunction by promoting SIRT1-mediated autophagy. Cell Mol Neurobiol 40(6):955–965. https://doi.org/10.1007/s10571-020-00786-6

    Article  CAS  PubMed  Google Scholar 

  77. Zhang S, Edelmann L, Liu J, Crandall JE, Morabito MA (2008) Cdk5 regulates the phosphorylation of tyrosine 1472 NR2B and the surface expression of NMDA receptors. J Neurosci 28(2):415–424. https://doi.org/10.1523/JNEUROSCI.1900-07.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Alves HN, da Silva AL, Olsson IA, Orden JM, Antunes LM (2010) Anesthesia with intraperitoneal propofol, medetomidine, and fentanyl in rats. J Am Assoc Lab Anim Sci 49(4):454–459

    PubMed  PubMed Central  Google Scholar 

  79. Dantzer R (2001) Cytokine-induced sickness behavior: mechanisms and implications. Ann N Y Acad Sci 933:222–234. https://doi.org/10.1111/j.1749-6632.2001.tb05827.x

    Article  CAS  PubMed  Google Scholar 

  80. Steffey MA, Brosnan RJ, Steffey EP (2003) Assessment of halothane and sevoflurane anesthesia in spontaneously breathing rats. Am J Vet Res 64(4):470–474. https://doi.org/10.2460/ajvr.2003.64.470

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Lixue Chen, Guangcheng Qing, and Dunke Zhang for their excellent technical assistance.

Funding

This study was supported by grants from the National Science Foundation Project of Chongqing (cstc2017jcyjBX0043 and cstc2019jcyj-msxmX0608).

Author information

Author notes

  1. Bo Chen and Bianqin Guo contributed equally to this work.

Authors and Affiliations

  1. Department of Anesthesiology, Chongqing University Cancer Hospital, Chongqing, 40030, People’s Republic of China

    Hongliang Liu, Bo Chen & Xiaoyuan Deng

  2. Department of Clinical Laboratory, Chongqing University Cancer Hospital, Chongqing, 40030, People’s Republic of China

    Bianqin Guo

  3. Institute of Life Sciences, Chongqing Medical University, Chongqing, 400016, People’s Republic of China

    Bin Wang & Xiaoyun Dou

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  3. Bianqin Guo
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  4. Xiaoyuan Deng
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  5. Bin Wang
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  6. Xiaoyun Dou
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Contributions

Bo Chen: conceptualization, methodology, formal analysis, investigation, writing–original draft, funding acquisition. Bianqin Guo: methodology, investigation. Xiaoyuan Deng: formal analysis, investigation, writing–original draft. Bin Wang: methodology, investigation, writing–review and editing. Xiaoyun Dou: investigation. Hongliang Liu: conceptualization, methodology, writing–original draft, writing–review and editing, funding acquisition.

Corresponding author

Correspondence to Hongliang Liu.

Ethics declarations

This study was conducted according to the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health (NIH) and the approval of the Committee on the Ethics of Animal Experiments of Chongqing University Cancer Hospital (Chongqing, P.R. China: Approval No. SCXK 2018-0003).

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The authors declare no competing interests.

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Bo Chen and Bianqin Guo are the co-first authors to this work.

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Liu, H., Chen, B., Guo, B. et al. Postconditioning with Sevoflurane or Propofol Alleviates Lipopolysaccharide-Induced Neuroinflammation but Exerts Dissimilar Effects on the NR2B Subunit and Cognition. Mol Neurobiol 58, 4251–4267 (2021). https://doi.org/10.1007/s12035-021-02402-0

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