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image of The Biological Changes of Synaptic Plasticity in the Pathological Process of Sepsis-associated Encephalopathy

Abstract

Sepsis-associated encephalopathy (SAE) is a form of cognitive and psychological impairment resulting from sepsis, which occurs without any central nervous system infection or structural brain injury. Patients may experience long-term cognitive deficits and psychiatric disorders even after discharge. However, the underlying mechanism remains unclear. As cognitive function and mental disease are closely related to synaptic plasticity, it is presumed that alterations in synaptic plasticity play an essential role in the pathological process of SAE. Here, we present a systematic description of the pathogenesis of SAE, which is primarily driven by glial cell activation and subsequent release of inflammatory mediators. Additionally, we elucidate the alterations in synaptic plasticity that occur during SAE and comprehensively discuss the roles played by glial cells and inflammatory factors in this process. In this review, we mainly discuss the synaptic plasticity of SAE, and the main aim is to show the consequences of SAE on inflammatory factors and how they affect synaptic plasticity. This review may enhance our understanding of the mechanism underlying cognitive dysfunction and provide valuable insights into identifying appropriate therapeutic targets for SAE.

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2024-10-28
2024-11-26

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References

  1. Singer M. Deutschman C.S. Seymour C.W. Shankar-Hari M. Annane D. Bauer M. Bellomo R. Bernard G.R. Chiche J.D. Coopersmith C.M. Hotchkiss R.S. Levy M.M. Marshall J.C. Martin G.S. Opal S.M. Rubenfeld G.D. van der Poll T. Vincent J.L. Angus D.C. The third in-ternational consensus definitions for sepsis and septic shock (sepsis-3). JAMA 2016 315 8 801 810 10.1001/jama.2016.0287 26903338
    [Google Scholar]
  2. Gofton T.E. Young G.B. Sepsis-associated encephalopathy. Nat. Rev. Neurol. 2012 8 10 557 566 10.1038/nrneurol.2012.183 22986430
    [Google Scholar]
  3. Robba C. Crippa I.A. Taccone F.S. Septic Encephalopathy. Curr. Neurol. Neurosci. Rep. 2018 18 12 82 10.1007/s11910‑018‑0895‑6 30280261
    [Google Scholar]
  4. Barichello T. Sayana P. Giridharan V.V. Arumanayagam A.S. Narendran B. Della Giustina A. Petronilho F. Que-vedo J. Dal-Pizzol F. Long-term cognitive outcomes after sepsis: A translational systematic review. Mol. Neurobiol. 2019 56 1 186 251 10.1007/s12035‑018‑1048‑2 29687346
    [Google Scholar]
  5. Iwashyna T.J. Ely E.W. Smith D.M. Langa K.M. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 2010 304 16 1787 1794 10.1001/jama.2010.1553 20978258
    [Google Scholar]
  6. Muzambi R. Bhaskaran K. Smeeth L. Brayne C. Chatur-vedi N. Warren-Gash C. Assessment of common infections and incident dementia using UK primary and secondary care data: A historical cohort study. Lancet Healthy Longev. 2021 2 7 e426 e435 10.1016/S2666‑7568(21)00118‑5 34240064
    [Google Scholar]
  7. Fritze T. Doblhammer G. Widmann C.N. Heneka M.T. Time course of dementia following sepsis in German health claims data. Neurol. Neuroimmunol. Neuroinflamm. 2021 8 1 e911 10.1212/NXI.0000000000000911 33293458
    [Google Scholar]
  8. Hell J.W. Binding of CaMKII to the NMDA receptor is suffi-cient for long-term potentiation. Sci. Signal. 2023 16 808 eadk9224 10.1126/scisignal.adk9224 37874884
    [Google Scholar]
  9. Magee J.C. Grienberger C. Synaptic plasticity forms and functions. Annu. Rev. Neurosci. 2020 43 1 95 117 10.1146/annurev‑neuro‑090919‑022842 32075520
    [Google Scholar]
  10. Takeuchi T. Duszkiewicz A.J. Morris R.G.M. The synaptic plasticity and memory hypothesis: encoding, storage and per-sistence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014 369 1633 20130288 10.1098/rstb.2013.0288 24298167
    [Google Scholar]
  11. Whitlock J.R. Heynen A.J. Shuler M.G. Bear M.F. Learn-ing induces long-term potentiation in the hippocampus. Science 2006 313 5790 1093 1097 10.1126/science.1128134 16931756
    [Google Scholar]
  12. Mazeraud A. Righy C. Bouchereau E. Benghanem S. Bozza F.A. Sharshar T. Septic-associated encephalopathy: A comprehensive review. Neurotherapeutics 2020 17 2 392 403 10.1007/s13311‑020‑00862‑1 32378026
    [Google Scholar]
  13. Catarina A.V. Branchini G. Bettoni L. De Oliveira J.R. Nunes F.B. Sepsis-associated encephalopathy: from patho-physiology to progress in experimental studies. Mol. Neurobiol. 2021 58 6 2770 2779 10.1007/s12035‑021‑02303‑2 33495934
    [Google Scholar]
  14. Li Y. Yin L. Fan Z. Su B. Chen Y. Ma Y. Zhong Y. Hou W. Fang Z. Zhang X. Microglia: A potential therapeu-tic target for sepsis-associated encephalopathy and sepsis-associated chronic pain. Front. Pharmacol. 2020 11 600421 10.3389/fphar.2020.600421 33329005
    [Google Scholar]
  15. Xin Y. Tian M. Deng S. Li J. Yang M. Gao J. Pei X. Wang Y. Tan J. Zhao F. Gao Y. Gong Y. The key driv-ers of brain injury by systemic inflammatory responses after sepsis: microglia and neuroinflammation. Mol. Neurobiol. 2023 60 3 1369 1390 10.1007/s12035‑022‑03148‑z 36445634
    [Google Scholar]
  16. Reyes E.P. Abarzúa S. Martin A. Rodríguez J. Cortés P.P. Fernández R. LPS-induced c-Fos activation in NTS neu-rons and plasmatic cortisol increases in septic rats are sup-pressed by bilateral carotid chemodenervation. Adv. Exp. Med. Biol. 2012 758 185 190 10.1007/978‑94‑007‑4584‑1_26 23080161
    [Google Scholar]
  17. Manabe T. Heneka M.T. Cerebral dysfunctions caused by sepsis during ageing. Nat. Rev. Immunol. 2022 22 7 444 458 10.1038/s41577‑021‑00643‑7 34764472
    [Google Scholar]
  18. He H. Geng T. Chen P. Wang M. Hu J. Kang L. Song W. Tang H. NK cells promote neutrophil recruitment in the brain during sepsis-induced neuroinflammation. Sci. Rep. 2016 6 1 27711 10.1038/srep27711 27270556
    [Google Scholar]
  19. Shulyatnikova T. Verkhratsky A. Astroglia in Sepsis Asso-ciated Encephalopathy. Neurochem. Res. 2020 45 1 83 99 10.1007/s11064‑019‑02743‑2 30778837
    [Google Scholar]
  20. Yan X. Yang K. Xiao Q. Hou R. Pan X. Zhu X. Central role of microglia in sepsis-associated encephalopathy: From mechanism to therapy. Front. Immunol. 2022 13 929316 10.3389/fimmu.2022.929316 35958583
    [Google Scholar]
  21. Cecconi M. Evans L. Levy M. Rhodes A. Sepsis and septic shock. Lancet 2018 392 10141 75 87 10.1016/S0140‑6736(18)30696‑2 29937192
    [Google Scholar]
  22. Vachharajani V. Cunningham C. Yoza B. Carson J. Jr Vachharajani T.J. McCall C. Adiponectin-deficiency exag-gerates sepsis-induced microvascular dysfunction in the mouse brain. Obesity (Silver Spring) 2012 20 3 498 504 10.1038/oby.2011.316 21996662
    [Google Scholar]
  23. Chapouly C. Tadesse Argaw A. Horng S. Castro K. Zhang J. Asp L. Loo H. Laitman B.M. Mariani J.N. Straus Farber R. Zaslavsky E. Nudelman G. Raine C.S. John G.R. Astrocytic TYMP and VEGFA drive blood–brain barrier opening in inflammatory central nervous system le-sions. Brain 2015 138 6 1548 1567 10.1093/brain/awv077 25805644
    [Google Scholar]
  24. Berg R.M.G. Møller K. Bailey D.M. Neuro-oxidative-nitrosative stress in sepsis. J. Cereb. Blood Flow Metab. 2011 31 7 1532 1544 10.1038/jcbfm.2011.48 21487413
    [Google Scholar]
  25. Bozza F.A. D’Avila J.C. Ritter C. Sonneville R. Sharshar T. Dal-Pizzol F. Bioenergetics, mitochondrial dysfunction, and oxidative stress in the pathophysiology of septic en-cephalopathy. Shock 2013 39 Suppl. 1 10 16 10.1097/SHK.0b013e31828fade1 23481496
    [Google Scholar]
  26. Calabrese V. Mancuso C. Calvani M. Rizzarelli E. Butter-field D.A. Giuffrida Stella A.M. Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 2007 8 10 766 775 10.1038/nrn2214 17882254
    [Google Scholar]
  27. Cesar Pontes Azevedo L. Mitochondrial dysfunction during sepsis. Endocr. Metab. Immune Disord. Drug Targets 2010 10 3 214 223 10.2174/187153010791936946 20509844
    [Google Scholar]
  28. Barichello T. Fortunato J.J. Vitali Â.M. Feier G. Reinke A. Moreira J.C.F. Quevedo J. Dal-Pizzol F. Oxidative vari-ables in the rat brain after sepsis induced by cecal ligation and perforation. Crit. Care Med. 2006 34 3 886 889 10.1097/01.CCM.0000201880.50116.12 16505668
    [Google Scholar]
  29. Xie K. Zhang Y. Wang Y. Meng X. Wang Y. Yu Y. Chen H. Hydrogen attenuates sepsis-associated encephalopa-thy by NRF2 mediated NLRP3 pathway inactivation. Inflamm. Res. 2020 69 7 697 710 10.1007/s00011‑020‑01347‑9 32350570
    [Google Scholar]
  30. Yu Y. Feng J. Lian N. Yang M. Xie K. Wang G. Wang C. Yu Y. Hydrogen gas alleviates blood-brain barrier im-pairment and cognitive dysfunction of septic mice in an Nrf2-dependent pathway. Int. Immunopharmacol. 2020 85 106585 10.1016/j.intimp.2020.106585 32447221
    [Google Scholar]
  31. Calabrese V. Cornelius C. Dinkova-Kostova A.T. Cala-brese E.J. Mattson M.P. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeu-tic intervention in neurodegenerative disorders. Antioxid. Redox Signal. 2010 13 11 1763 1811 10.1089/ars.2009.3074 20446769
    [Google Scholar]
  32. Calabrese V. Cornelius C. Dinkova-Kostova A.T. Cala-brese E.J. Vitagenes, cellular stress response, and acetyl-carnitine: Relevance to hormesis. Biofactors 2009 35 2 146 160 10.1002/biof.22 19449442
    [Google Scholar]
  33. Wang Z. Liu L. Liu L. Vitamin C as a treatment for organ failure in sepsis. Eur. J. Med. Res. 2023 28 1 222 10.1186/s40001‑023‑01183‑7 37408078
    [Google Scholar]
  34. Zhang N. Zhao W. Hu Z.J. Ge S.M. Huo Y. Liu L.X. Gao B.L. Protective effects and mechanisms of high-dose vitamin C on sepsis-associated cognitive impairment in rats. Sci. Rep. 2021 11 1 14511 10.1038/s41598‑021‑93861‑x 34267240
    [Google Scholar]
  35. Park J.E. Shin T.G. Jo I.J. Jeon K. Suh G.Y. Park M. Won H. Chung C.R. Hwang S.Y. Impact of vitamin C and thiamine administration on delirium-free days in patients with septic shock. J. Clin. Med. 2020 9 1 193 10.3390/jcm9010193 31936824
    [Google Scholar]
  36. Zhai Q. Lai D. Cui P. Zhou R. Chen Q. Hou J. Su Y. Pan L. Ye H. Zhao J.W. Fang X. Selective activation of basal forebrain cholinergic neurons attenuates polymicrobial sepsis-induced inflammation via the cholinergic anti-inflammatory pathway. Crit. Care Med. 2017 45 10 e1075 e1082 10.1097/CCM.0000000000002646 28806219
    [Google Scholar]
  37. Collingridge G.L. Abraham W.C. Glutamate receptors and synaptic plasticity: The impact of evans and watkins. Neuropharmacology 2022 206 108922 10.1016/j.neuropharm.2021.108922 34919905
    [Google Scholar]
  38. Park M. AMPA receptor trafficking for postsynaptic potentia-tion. Front. Cell. Neurosci. 2018 12 361 10.3389/fncel.2018.00361 30364291
    [Google Scholar]
  39. Nicoll R.A. Schulman H. Synaptic memory and CaMKII. Physiol. Rev. 2023 103 4 2897 2945 10.1152/physrev.00034.2022 37290118
    [Google Scholar]
  40. Scheff S.W. Price D.A. Schmitt F.A. DeKosky S.T. Mufson E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 2007 68 18 1501 1508 10.1212/01.wnl.0000260698.46517.8f 17470753
    [Google Scholar]
  41. Vanhaute H. Ceccarini J. Michiels L. Koole M. Sunaert S. Lemmens R. Triau E. Emsell L. Vandenbulcke M. Van Laere K. In vivo synaptic density loss is related to tau deposition in amnestic mild cognitive impairment. Neurology 2020 95 5 e545 e553 10.1212/WNL.0000000000009818 32493717
    [Google Scholar]
  42. Robinson J.L. Molina-Porcel L. Corrada M.M. Raible K. Lee E.B. Lee V.M.Y. Kawas C.H. Trojanowski J.Q. Per-forant path synaptic loss correlates with cognitive impairment and Alzheimer’s disease in the oldest-old. Brain 2014 137 9 2578 2587 10.1093/brain/awu190 25012223
    [Google Scholar]
  43. Manabe T. Rácz I. Schwartz S. Oberle L. Santarelli F. Emmrich J.V. Neher J.J. Heneka M.T. Systemic inflamma-tion induced the delayed reduction of excitatory synapses in the CA3 during ageing. J. Neurochem. 2021 159 3 525 542 10.1111/jnc.15491 34379806
    [Google Scholar]
  44. Song Z. Shen F. Zhang Z. Wu S. Zhu G. Calpain inhibi-tion ameliorates depression-like behaviors by reducing in-flammation and promoting synaptic protein expression in the hippocampus. Neuropharmacology 2020 174 108175 10.1016/j.neuropharm.2020.108175 32492450
    [Google Scholar]
  45. Kondo S. Kohsaka S. Okabe S. Long-term changes of spine dynamics and microglia after transient peripheral im-mune response triggered by LPS in vivo. Mol. Brain 2011 4 1 27 10.1186/1756‑6606‑4‑27 21682853
    [Google Scholar]
  46. Hosseini S. Wilk E. Michaelsen-Preusse K. Gerhauser I. Baumgärtner W. Geffers R. Schughart K. Korte M. Long-term neuroinflammation induced by influenza a virus infec-tion and the impact on hippocampal neuron morphology and function. J. Neurosci. 2018 38 12 3060 3080 10.1523/JNEUROSCI.1740‑17.2018 29487124
    [Google Scholar]
  47. Zhang J. Malik A. Choi H.B. Ko R.W.Y. Dissing-Olesen L. MacVicar B.A. Microglial CR3 activation triggers long-term synaptic depression in the hippocampus via NADPH ox-idase. Neuron 2014 82 1 195 207 10.1016/j.neuron.2014.01.043 24631344
    [Google Scholar]
  48. Moraes C.A. Santos G. Spohr T.C.L.S. D’Avila J.C. Lima F.R.S. Benjamim C.F. Bozza F.A. Gomes F.C.A. Activated microglia-induced deficits in excitatory synapses through IL-1β: implications for cognitive impairment in sep-sis. Mol. Neurobiol. 2015 52 1 653 663 10.1007/s12035‑014‑8868‑5 25257696
    [Google Scholar]
  49. Chung H.Y. Wickel J. Hahn N. Mein N. Schwarzbrunn M. Koch P. Ceanga M. Haselmann H. Baade-Büttner C. von Stackelberg N. Hempel N. Schmidl L. Groth M. An-dreas N. Götze J. Coldewey S.M. Bauer M. Mawrin C. Dargvainiene J. Leypoldt F. Steinke S. Wang Z.Q. Hust M. Geis C. Microglia mediate neurocognitive deficits by eliminating C1q-tagged synapses in sepsis-associated enceph-alopathy. Sci. Adv. 2023 9 21 eabq7806 10.1126/sciadv.abq7806 37235660
    [Google Scholar]
  50. Jiang J. Zou Y. Xie C. Yang M. Tong Q. Yuan M. Pei X. Deng S. Tian M. Xiao L. Gong Y. Oxytocin alleviates cognitive and memory impairments by decreasing hippocam-pal microglial activation and synaptic defects via OXTR/ERK/STAT3 pathway in a mouse model of sepsis-associated encephalopathy. Brain Behav. Immun. 2023 114 195 213 10.1016/j.bbi.2023.08.023 37648002
    [Google Scholar]
  51. Bluemel P. Wickel J. Grünewald B. Ceanga M. Keiner S. Witte O.W. Redecker C. Geis C. Kunze A. Sepsis pro-motes gliogenesis and depletes the pool of radial glia like stem cells in the hippocampus. Exp. Neurol. 2021 338 113591 10.1016/j.expneurol.2020.113591 33387461
    [Google Scholar]
  52. Beyer M.M.S. Lonnemann N. Remus A. Latz E. Heneka M.T. Korte M. Enduring Changes in neuronal function upon systemic inflammation are NLRP3 inflammasome dependent. J. Neurosci. 2020 40 28 5480 5494 10.1523/JNEUROSCI.0200‑20.2020 32499379
    [Google Scholar]
  53. Qin Z. Zhou C. Xiao X. Guo C. Metformin attenuates sepsis-induced neuronal injury and cognitive impairment. BMC Neurosci. 2021 22 1 78 10.1186/s12868‑021‑00683‑8 34911449
    [Google Scholar]
  54. Zivkovic A.R. Sedlaczek O. Von Haken R. Schmidt K. Brenner T. Weigand M.A. Bading H. Bengtson C.P. Ho-fer S. Muscarinic M1 receptors modulate endotoxemia-induced loss of synaptic plasticity. Acta Neuropathol. Commun. 2015 3 67 10.1186/s40478‑015‑0245‑8 26531194
    [Google Scholar]
  55. Stachowicz K. Pańczyszyn-Trzewik P. Sowa-Kućma M. Misztak P. Changes in working memory induced by lipopol-ysaccharide administration in mice are associated with metabotropic glutamate receptors 5 and contrast with changes induced by cyclooxygenase-2: Involvement of postsynaptic density protein 95 and down syndrome cell adhesion mole-cule. Neuropeptides 2023 100 102347 10.1016/j.npep.2023.102347 37182274
    [Google Scholar]
  56. Yang S. Seo H. Wang M. Arnsten A.F.T. NMDAR neuro-transmission needed for persistent neuronal firing: Potential roles in mental disorders. Front. Psychiatry 2021 12 654322 10.3389/fpsyt.2021.654322 33897503
    [Google Scholar]
  57. Zong M. Yuan H. He X. Zhou Z. Qiu X. Yang J. Ji M. Disruption of striatal-enriched protein tyrosine phosphatase signaling might contribute to memory impairment in a mouse model of sepsis-associated encephalopathy. Neurochem. Res. 2019 44 12 2832 2842 10.1007/s11064‑019‑02905‑2 31691882
    [Google Scholar]
  58. Tauber S.C. Djukic M. Gossner J. Eiffert H. Brück W. Nau R. Sepsis-associated encephalopathy and septic en-cephalitis: An update. Expert Rev. Anti Infect. Ther. 2021 19 2 215 231 10.1080/14787210.2020.1812384 32808580
    [Google Scholar]
  59. Tang C. Jin Y. Wang H. The biological alterations of syn-apse/synapse formation in sepsis-associated encephalopathy. Front. Synaptic Neurosci. 2022 14 1054605 10.3389/fnsyn.2022.1054605 36530954
    [Google Scholar]
  60. Peters van Ton A.M. Verbeek M.M. Alkema W. Pickkers P. Abdo W.F. Downregulation of synapse-associated protein expression and loss of homeostatic microglial control in cere-brospinal fluid of infectious patients with delirium and pa-tients with Alzheimer’s disease. Brain Behav. Immun. 2020 89 656 667 10.1016/j.bbi.2020.06.027 32592865
    [Google Scholar]
  61. Jiang P.P. Peng S.S. Pankratova S. Luo P. Zhou P. Chen Y. Proteins involved in synaptic plasticity are down-regulated in the cerebrospinal fluid of infants with clinical sepsis complicated by neuroinflammation. Front. Cell. Neurosci. 2022 16 887212 10.3389/fncel.2022.887212 35634471
    [Google Scholar]
  62. Sancho L. Contreras M. Allen N.J. Glia as sculptors of synaptic plasticity. Neurosci. Res. 2021 167 17 29 10.1016/j.neures.2020.11.005 33316304
    [Google Scholar]
  63. Andoh M. Koyama R. Microglia regulate synaptic develop-ment and plasticity. Dev. Neurobiol. 2021 81 5 568 590 10.1002/dneu.22814 33583110
    [Google Scholar]
  64. Wilton D.K. Dissing-Olesen L. Stevens B. Neuron-Glia Signaling in Synapse Elimination. Annu. Rev. Neurosci. 2019 42 1 107 127 10.1146/annurev‑neuro‑070918‑050306 31283900
    [Google Scholar]
  65. Vukojicic A. Delestrée N. Fletcher E.V. Pagiazitis J.G. Sankaranarayanan S. Yednock T.A. Barres B.A. Mentis G.Z. The classical complement pathway mediates microglia-dependent remodeling of spinal motor circuits during devel-opment and in SMA. Cell Rep. 2019 29 10 3087 3100.e7 10.1016/j.celrep.2019.11.013 31801075
    [Google Scholar]
  66. Xin Y.R. Jiang J.X. Hu Y. Pan J.P. Mi X.N. Gao Q. Xiao F. Zhang W. Luo H.M. The immune system drives synapse loss during Lipopolysaccharide-induced learning and memory impairment in mice. Front. Aging Neurosci. 2019 11 279 10.3389/fnagi.2019.00279 31803043
    [Google Scholar]
  67. Cangalaya C. Wegmann S. Sun W. Diez L. Gottfried A. Richter K. Stoyanov S. Pakan J. Fischer K.D. Dityatev A. Real-time mechanisms of exacerbated synaptic remodeling by microglia in acute models of systemic inflammation and tauopathy. Brain Behav. Immun. 2023 110 245 259 10.1016/j.bbi.2023.02.023 36906076
    [Google Scholar]
  68. Stephan A.H. Barres B.A. Stevens B. The complement system: An unexpected role in synaptic pruning during devel-opment and disease. Annu. Rev. Neurosci. 2012 35 1 369 389 10.1146/annurev‑neuro‑061010‑113810 22715882
    [Google Scholar]
  69. Vasek M.J. Garber C. Dorsey D. Durrant D.M. Bollman B. Soung A. Yu J. Perez-Torres C. Frouin A. Wilton D.K. Funk K. DeMasters B.K. Jiang X. Bowen J.R. Mennerick S. Robinson J.K. Garbow J.R. Tyler K.L. Suthar M.S. Schmidt R.E. Stevens B. Klein R.S. A com-plement–microglial axis drives synapse loss during virus-induced memory impairment. Nature 2016 534 7608 538 543 10.1038/nature18283 27337340
    [Google Scholar]
  70. Scott-Hewitt N. Perrucci F. Morini R. Erreni M. Ma-honey M. Witkowska A. Carey A. Faggiani E. Schuetz L.T. Mason S. Tamborini M. Bizzotto M. Passoni L. Fil-ipello F. Jahn R. Stevens B. Matteoli M. Local externali-zation of phosphatidylserine mediates developmental synaptic pruning by microglia. EMBO J. 2020 39 16 e105380 10.15252/embj.2020105380 32657463
    [Google Scholar]
  71. Filipello F. Morini R. Corradini I. Zerbi V. Canzi A. Michalski B. Erreni M. Markicevic M. Starvaggi-Cucuzza C. Otero K. Piccio L. Cignarella F. Perrucci F. Tambo-rini M. Genua M. Rajendran L. Menna E. Vetrano S. Fahnestock M. Paolicelli R.C. Matteoli M. The microglial innate immune receptor TREM2 is required for synapse elim-ination and normal brain connectivity. Immunity 2018 48 5 979 991.e8 10.1016/j.immuni.2018.04.016 29752066
    [Google Scholar]
  72. Danielski L.G. Giustina A.D. Goldim M.P. Florentino D. Mathias K. Garbossa L. de Bona Schraiber R. Laurentino A.O.M. Goulart M. Michels M. de Queiroz K.B. Kohlhof M. Rezin G.T. Fortunato J.J. Quevedo J. Barichello T. Dal-Pizzol F. Coimbra R.S. Petronilho F. Vitamin B6 re-duces neurochemical and long-term cognitive alterations after polymicrobial sepsis: Involvement of the kynurenine pathway modulation. Mol. Neurobiol. 2018 55 6 5255 5268 10.1007/s12035‑017‑0706‑0 28879460
    [Google Scholar]
  73. Païdassi H. Tacnet-Delorme P. Garlatti V. Darnault C. Ghebrehiwet B. Gaboriaud C. Arlaud G.J. Frachet P. C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J. Immunol. 2008 180 4 2329 2338 10.4049/jimmunol.180.4.2329 18250442
    [Google Scholar]
  74. Li S. Li B. Zhang L. Zhang G. Sun J. Ji M. Yang J. A complement-microglial axis driving inhibitory synapse related protein loss might contribute to systemic inflammation-induced cognitive impairment. Int. Immunopharmacol. 2020 87 106814 10.1016/j.intimp.2020.106814 32707491
    [Google Scholar]
  75. Weinhard L. di Bartolomei G. Bolasco G. Machado P. Schieber N.L. Neniskyte U. Exiga M. Vadisiute A. Rag-gioli A. Schertel A. Schwab Y. Gross C.T. Microglia re-model synapses by presynaptic trogocytosis and spine head filopodia induction. Nat. Commun. 2018 9 1 1228 10.1038/s41467‑018‑03566‑5 29581545
    [Google Scholar]
  76. Kettenmann H. Kirchhoff F. Verkhratsky A. Microglia: new roles for the synaptic stripper. Neuron 2013 77 1 10 18 10.1016/j.neuron.2012.12.023 23312512
    [Google Scholar]
  77. Prada I. Gabrielli M. Turola E. Iorio A. D’Arrigo G. Parolisi R. De Luca M. Pacifici M. Bastoni M. Lombardi M. Legname G. Cojoc D. Buffo A. Furlan R. Peruzzi F. Verderio C. Glia-to-neuron transfer of miRNAs via extracel-lular vesicles: a new mechanism underlying inflammation-induced synaptic alterations. Acta Neuropathol. 2018 135 4 529 550 10.1007/s00401‑017‑1803‑x 29302779
    [Google Scholar]
  78. Moraes C.A. Hottz E.D. Dos Santos Ornellas D. Adesse D. de Azevedo C.T. d’Avila J.C. Zaverucha-do-Valle C. Maron-Gutierrez T. Barbosa H.S. Bozza P.T. Bozza F.A. Microglial NLRP3 Inflammasome Induces Excitatory Synap-tic Loss Through IL-1β-Enriched Microvesicle Release: Im-plications for Sepsis-Associated Encephalopathy. Mol. Neurobiol. 2023 60 2 481 494 10.1007/s12035‑022‑03067‑z 36280654
    [Google Scholar]
  79. Han Q. Lin Q. Huang P. Chen M. Hu X. Fu H. He S. Shen F. Zeng H. Deng Y. Microglia-derived IL-1β contrib-utes to axon development disorders and synaptic deficit through p38-MAPK signal pathway in septic neonatal rats. J. Neuroinflammation 2017 14 1 52 10.1186/s12974‑017‑0805‑x 28288671
    [Google Scholar]
  80. Ito H. Hosomi S. Koyama Y. Matsumoto H. Imamura Y. Ogura H. Oda J. Sepsis-associated encephalopathy: A mini-review of inflammation in the brain and body. Front. Aging Neurosci. 2022 14 912866 10.3389/fnagi.2022.912866 35711904
    [Google Scholar]
  81. Sheppard O. Coleman M.P. Durrant C.S. Lipopolysaccha-ride-induced neuroinflammation induces presynaptic disrup-tion through a direct action on brain tissue involving micro-glia-derived interleukin 1 beta. J. Neuroinflammation 2019 16 1 106 10.1186/s12974‑019‑1490‑8 31103036
    [Google Scholar]
  82. Lim S.H. Park E. You B. Jung Y. Park A.R. Park S.G. Lee J.R. Neuronal synapse formation induced by microglia and interleukin 10. PLoS One 2013 8 11 e81218 10.1371/journal.pone.0081218 24278397
    [Google Scholar]
  83. Richwine A.F. Sparkman N.L. Dilger R.N. Buchanan J.B. Johnson R.W. Cognitive deficits in interleukin-10-deficient mice after peripheral injection of lipopolysaccharide. Brain Behav. Immun. 2009 23 6 794 802 10.1016/j.bbi.2009.02.020 19272439
    [Google Scholar]
  84. Welser-Alves J.V. Milner R. Microglia are the major source of TNF-α and TGF-β1 in postnatal glial cultures; regulation by cytokines, lipopolysaccharide, and vitronectin. Neurochem. Int. 2013 63 1 47 53 10.1016/j.neuint.2013.04.007 23619393
    [Google Scholar]
  85. Zipp F. Bittner S. Schafer D.P. Cytokines as emerging regulators of central nervous system synapses. Immunity 2023 56 5 914 925 10.1016/j.immuni.2023.04.011 37163992
    [Google Scholar]
  86. Mao Y. Zhang A. Yang H. Zhang C. Identification of IL-8 in CSF as a potential biomarker in sepsis-associated encepha-lopathy. Cytokine 2023 172 156390 10.1016/j.cyto.2023.156390 37812997
    [Google Scholar]
  87. Mégarbane B. Marchal P. Marfaing-Koka A. Belliard O. Jacobs F. Chary I. Brivet F.G. Increased diffusion of solu-ble adhesion molecules in meningitis, severe sepsis and sys-temic inflammatory response without neurological infection is associated with intrathecal shedding in cases of meningitis. Intensive Care Med. 2004 30 5 867 874 10.1007/s00134‑004‑2253‑1 15067502
    [Google Scholar]
  88. Momonaka H. Hasegawa S. Matsushige T. Inoue H. Kajimoto M. Okada S. Nakatsuka K. Morishima T. Ichiyama T. High mobility group box 1 in patients with 2009 pandemic H1N1 influenza-associated encephalopathy. Brain Dev. 2014 36 6 484 488 10.1016/j.braindev.2013.07.001 23907181
    [Google Scholar]
  89. Hasegawa-Ishii S. Inaba M. Shimada A. Widespread time-dependent changes in tissue cytokine concentrations in brain regions during the acute phase of endotoxemia in mice. Neurotoxicology 2020 76 67 74 10.1016/j.neuro.2019.10.006 31628962
    [Google Scholar]
  90. Lynch M.A. Neuroinflammatory changes negatively impact on LTP: A focus on IL-1β. Brain Res. 2015 1621 197 204 10.1016/j.brainres.2014.08.040 25193603
    [Google Scholar]
  91. Avital A. Goshen I. Kamsler A. Segal M. Iverfeldt K. Richter-Levin G. Yirmiya R. Impaired interleukin‐1 signal-ing is associated with deficits in hippocampal memory pro-cesses and neural plasticity. Hippocampus 2003 13 7 826 834 10.1002/hipo.10135 14620878
    [Google Scholar]
  92. Wang P. Rothwell N.J. Pinteaux E. Brough D. Neuronal injury induces the release of pro-interleukin-1β from activat-ed microglia in vitro. Brain Res. 2008 1236 1 7 10.1016/j.brainres.2008.08.001 18722361
    [Google Scholar]
  93. Imamura Y. Wang H. Matsumoto N. Muroya T. Shima-zaki J. Ogura H. Shimazu T. Interleukin-1β causes long-term potentiation deficiency in a mouse model of septic en-cephalopathy. Neuroscience 2011 187 63 69 10.1016/j.neuroscience.2011.04.063 21571042
    [Google Scholar]
  94. Zhang R. Sun L. Hayashi Y. Liu X. Koyama S. Wu Z. Nakanishi H. Acute p38-mediated inhibition of NMDA-induced outward currents in hippocampal CA1 neurons by in-terleukin-1β. Neurobiol. Dis. 2010 38 1 68 77 10.1016/j.nbd.2009.12.028 20060906
    [Google Scholar]
  95. Mishra A. Kim H.J. Shin A.H. Thayer S.A. Synapse loss induced by interleukin-1β requires pre- and post-synaptic mechanisms. J. Neuroimmune Pharmacol. 2012 7 3 571 578 10.1007/s11481‑012‑9342‑7 22311599
    [Google Scholar]
  96. Bellingacci L. Canonichesi J. Mancini A. Parnetti L. Di Filippo M. Cytokines, synaptic plasticity and network dy-namics: A matter of balance. Neural Regen. Res. 2023 18 12 2569 2572 10.4103/1673‑5374.371344 37449591
    [Google Scholar]
  97. Serantes R. Arnalich F. Figueroa M. Salinas M. Andrés-Mateos E. Codoceo R. Renart J. Matute C. Cavada C. Cuadrado A. Montiel C. Interleukin-1β enhances GABAA receptor cell-surface expression by a phosphatidylinositol 3-kinase/Akt pathway: Relevance to sepsis-associated encepha-lopathy. J. Biol. Chem. 2006 281 21 14632 14643 10.1074/jbc.M512489200 16567807
    [Google Scholar]
  98. Wang D.S. Zurek A.A. Lecker I. Yu J. Abramian A.M. Avramescu S. Davies P.A. Moss S.J. Lu W.Y. Orser B.A. Memory deficits induced by inflammation are regulated by α5-subunit-containing GABAA receptors. Cell Rep. 2012 2 3 488 496 10.1016/j.celrep.2012.08.022 22999935
    [Google Scholar]
  99. Murdaca G. Paladin F. Casciaro M. Vicario C.M. Gan-gemi S. Martino G. Neuro-inflammaging and psychopatho-logical distress. Biomedicines 2022 10 9 2133 10.3390/biomedicines10092133 36140234
    [Google Scholar]
  100. Tang D. Kang R. Zeh H.J. Lotze M.T. The multifunctional protein HMGB1: 50 years of discovery. Nat. Rev. Immunol. 2023 23 12 824 841 10.1038/s41577‑023‑00894‑6 37322174
    [Google Scholar]
  101. Sundén-Cullberg J. Norrby-Teglund A. Rouhiainen A. Rauvala H. Herman G. Tracey K.J. Lee M.L. Andersson J. Tokics L. Treutiger C.J. Persistent elevation of high mo-bility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock. Crit. Care Med. 2005 33 3 564 573 10.1097/01.CCM.0000155991.88802.4D 15753748
    [Google Scholar]
  102. Frank M.G. Weber M.D. Watkins L.R. Maier S.F. Stress sounds the alarmin: The role of the danger-associated mo-lecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav. Immun. 2015 48 1 7 10.1016/j.bbi.2015.03.010 25816800
    [Google Scholar]
  103. Franklin T.C. Wohleb E.S. Zhang Y. Fogaça M. Hare B. Duman R.S. Persistent increase in microglial RAGE contrib-utes to chronic stress–induced priming of depressive-like be-havior. Biol. Psychiatry 2018 83 1 50 60 10.1016/j.biopsych.2017.06.034 28882317
    [Google Scholar]
  104. Wang B. Huang X. Pan X. Zhang T. Hou C. Su W.J. Liu L.L. Li J.M. Wang Y.X. Minocycline prevents the de-pressive-like behavior through inhibiting the release of HMGB1 from microglia and neurons. Brain Behav. Immun. 2020 88 132 143 10.1016/j.bbi.2020.06.019 32553784
    [Google Scholar]
  105. Xiong Y. Yang J. Tong H. Zhu C. Pang Y. HMGB1 augments cognitive impairment in sepsis‐associated encepha-lopathy by binding to MD ‐2 and promoting NLRP3 ‐induced neuroinflammation. Psychogeriatrics 2022 22 2 167 179 10.1111/psyg.12794 34931753
    [Google Scholar]
  106. Xin Y. Wang J. Chu T. Zhou Y. Liu C. Xu A. Electro-acupuncture alleviates neuroinflammation by inhibiting the HMGB1 signaling pathway in rats with sepsis-associated en-cephalopathy. Brain Sci. 2022 12 12 1732 10.3390/brainsci12121732 36552192
    [Google Scholar]
  107. Valdés-Ferrer S.I. Rosas-Ballina M. Olofsson P.S. Lu B. Dancho M.E. Li J. Yang H. Pavlov V.A. Chavan S.S. Tracey K.J. High-mobility group box 1 mediates persistent splenocyte priming in sepsis survivors: Evidence from a mu-rine model. Shock 2013 40 6 492 495 10.1097/SHK.0000000000000050 24089009
    [Google Scholar]
  108. Yin X.Y. Tang X.H. Wang S.X. Zhao Y.C. Jia M. Yang J.J. Ji M.H. Shen J.C. HMGB1 mediates synaptic loss and cognitive impairment in an animal model of sepsis-associated encephalopathy. J. Neuroinflammation 2023 20 1 69 10.1186/s12974‑023‑02756‑3 36906561
    [Google Scholar]
  109. Chavan S.S. Huerta P.T. Robbiati S. Valdes-Ferrer S.I. Ochani M. Dancho M. Frankfurt M. Volpe B.T. Tracey K.J. Diamond B. HMGB1 mediates cognitive impairment in sepsis survivors. Mol. Med. 2012 18 6 930 937 10.2119/molmed.2012.00195 22634723
    [Google Scholar]
  110. Dal-Pizzol F. Pasquali M. Quevedo J. Gelain D.P. Moreira J.C.F. Is there a role for high mobility group box 1 and the receptor for advanced glycation end products in the genesis of long-term cognitive impairment in sepsis survi-vors? Mol. Med. 2012 18 10 1357 1358 10.2119/molmed.2012.00317 23114886
    [Google Scholar]
  111. Matsumoto H. Matsumoto N. Ogura H. Shimazaki J. Yamakawa K. Yamamoto K. Shimazu T. The clinical sig-nificance of circulating soluble RAGE in patients with severe sepsis. J. Trauma Acute Care Surg. 2015 78 6 1086 1094 10.1097/TA.0000000000000651 26002402
    [Google Scholar]
  112. Nogueira-Machado J.A. de Oliveira Volpe C.M. HMGB-1 as a target for inflammation controlling. Recent Pat. Endocr. Metab. Immune Drug Discov. 2012 6 3 201 209 10.2174/187221412802481784 22845335
    [Google Scholar]
  113. Wang H. Tang Y. Fan Z. Lv B. Xiao X. Chen F. High-mobility group box 1 protein induces tissue factor expression in vascular endothelial cells via activation of NF-κB and Egr-1. Thromb. Haemost. 2009 102 8 352 359 10.1160/TH08‑11‑0759 19652887
    [Google Scholar]
  114. Gasparotto J. Girardi C.S. Somensi N. Ribeiro C.T. Moreira J.C.F. Michels M. Sonai B. Rocha M. Steckert A.V. Barichello T. Quevedo J. Dal-Pizzol F. Gelain D.P. Receptor for advanced glycation end products mediates sep-sis-triggered amyloid-β accumulation, Tau phosphorylation, and cognitive impairment. J. Biol. Chem. 2018 293 1 226 244 10.1074/jbc.M117.786756 29127203
    [Google Scholar]
  115. Shi J. Xu H. Cavagnaro M.J. Li X. Fang J. Blocking HMGB1/RAGE signaling by berberine alleviates A1 astrocyte and attenuates sepsis-associated encephalopathy. Front. Pharmacol. 2021 12 760186 10.3389/fphar.2021.760186 34867376
    [Google Scholar]
  116. Turrigiano G.G. Leslie K.R. Desai N.S. Rutherford L.C. Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998 391 6670 892 896 10.1038/36103 9495341
    [Google Scholar]
  117. Rizzo F.R. Musella A. De Vito F. Fresegna D. Bullitta S. Vanni V. Guadalupi L. Stampanoni Bassi M. Buttari F. Mandolesi G. Centonze D. Gentile A. Tumor necrosis fac-tor and interleukin-1 β modulate synaptic plasticity during Neuroinflammation. Neural Plast. 2018 2018 1 12 10.1155/2018/8430123 29861718
    [Google Scholar]
  118. Calsavara A.C. Soriani F.M. Vieira L.Q. Costa P.A. Ra-chid M.A. Teixiera A.L. TNFR1 absence protects against memory deficit induced by sepsis possibly through over-expression of hippocampal BDNF. Metab. Brain Dis. 2015 30 3 669 678 10.1007/s11011‑014‑9610‑8 25148914
    [Google Scholar]
  119. Tian L. Stefanidakis M. Ning L. Van Lint P. Nyman-Huttunen H. Libert C. Itohara S. Mishina M. Rauvala H. Gahmberg C.G. Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J. Cell Biol. 2007 178 4 687 700 10.1083/jcb.200612097 17682049
    [Google Scholar]
  120. Paetau S. Rolova T. Ning L. Gahmberg C.G. Neuronal ICAM-5 inhibits microglia adhesion and phagocytosis and promotes an anti-inflammatory response in LPS stimulated microglia. Front. Mol. Neurosci. 2017 10 431 10.3389/fnmol.2017.00431 29311819
    [Google Scholar]
  121. Gahmberg C.G. Ning L. Paetau S. ICAM-5: A neuronal dendritic adhesion molecule involved in immune and neu-ronal functions. Adv. Neurobiol. 2014 8 117 132 10.1007/978‑1‑4614‑8090‑7_6 25300135
    [Google Scholar]
  122. Gyoneva S. Traynelis S.F. Norepinephrine modulates the motility of resting and activated microglia via different adren-ergic receptors. J. Biol. Chem. 2013 288 21 15291 15302 10.1074/jbc.M113.458901 23548902
    [Google Scholar]
  123. Stowell R.D. Sipe G.O. Dawes R.P. Batchelor H.N. Lordy K.A. Whitelaw B.S. Stoessel M.B. Bidlack J.M. Brown E. Sur M. Majewska A.K. Noradrenergic signaling in the wakeful state inhibits microglial surveillance and syn-aptic plasticity in the mouse visual cortex. Nat. Neurosci. 2019 22 11 1782 1792 10.1038/s41593‑019‑0514‑0 31636451
    [Google Scholar]
  124. Zong M.M. Zhou Z.Q. Ji M.H. Jia M. Tang H. Yang J.J. Activation of β2-adrenoceptor attenuates sepsis-induced hip-pocampus-dependent cognitive impairments by reversing neuroinflammation and synaptic abnormalities. Front. Cell. Neurosci. 2019 13 293 10.3389/fncel.2019.00293 31354429
    [Google Scholar]
  125. Xu X. Liu L. Wang Y. Wang C. Zheng Q. Liu Q. Li Z. Bai X. Liu X. Caspase-1 inhibitor exerts brain-protective effects against sepsis-associated encephalopathy and cogni-tive impairments in a mouse model of sepsis. Brain Behav. Immun. 2019 80 859 870 10.1016/j.bbi.2019.05.038 31145977
    [Google Scholar]
  126. Garrido-Mesa N. Zarzuelo A. Gálvez J. Minocycline: far beyond an antibiotic. Br. J. Pharmacol. 2013 169 2 337 352 10.1111/bph.12139 23441623
    [Google Scholar]
  127. Michels M. Vieira A.S. Vuolo F. Zapelini H.G. Mendon-ça B. Mina F. Dominguini D. Steckert A. Schuck P.F. Quevedo J. Petronilho F. Dal-Pizzol F. The role of micro-glia activation in the development of sepsis-induced long-term cognitive impairment. Brain Behav. Immun. 2015 43 54 59 10.1016/j.bbi.2014.07.002 25019583
    [Google Scholar]
  128. Hoshino K. Hayakawa M. Morimoto Y. Minocycline pre-vents the impairment of hippocampal long-term potentiation in the septic mouse. Shock 2017 48 2 209 214 10.1097/SHK.0000000000000847 28187038
    [Google Scholar]
  129. Henry C.J. Huang Y. Wynne A. Hanke M. Himler J. Bailey M.T. Sheridan J.F. Godbout J.P. Minocycline atten-uates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J. Neuroinflammation 2008 5 1 15 10.1186/1742‑2094‑5‑15 18477398
    [Google Scholar]
  130. Tomás-Camardiel M. Rite I. Herrera A.J. de Pablos R.M. Cano J. Machado A. Venero J.L. Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxyni-trite-mediated nitration of proteins, disruption of the blood–brain barrier, and damage in the nigral dopaminergic system. Neurobiol. Dis. 2004 16 1 190 201 10.1016/j.nbd.2004.01.010 15207276
    [Google Scholar]
  131. Liu Y. Zhang Y. Zheng X. Fang T. Yang X. Luo X. Guo A. Newell K.A. Huang X.F. Yu Y. Galantamine im-proves cognition, hippocampal inflammation, and synaptic plasticity impairments induced by lipopolysaccharide in mice. J. Neuroinflammation 2018 15 1 112 10.1186/s12974‑018‑1141‑5 29669582
    [Google Scholar]
  132. Wu X. Liu C. Chen L. Du Y.F. Hu M. Reed M.N. Long Y. Suppiramaniam V. Hong H. Tang S.S. Protective effects of tauroursodeoxycholic acid on lipopolysaccharide-induced cognitive impairment and neurotoxicity in mice. Int. Immunopharmacol. 2019 72 166 175 10.1016/j.intimp.2019.03.065 30986644
    [Google Scholar]
  133. Im H. Ju I.G. Kim J.H. Lee S. Oh M.S. Trichosanthis semen and zingiberis rhizoma mixture ameliorates lipopoly-saccharide-induced memory dysfunction by inhibiting neu-roinflammation. Int. J. Mol. Sci. 2022 23 22 14015 10.3390/ijms232214015 36430493
    [Google Scholar]
  134. van Praag H. Kempermann G. Gage F.H. Neural conse-quences of enviromental enrichment. Nat. Rev. Neurosci. 2000 1 3 191 198 10.1038/35044558 11257907
    [Google Scholar]
  135. Wu X. Ji M. Yin X. Gu H. Zhu T. Wang R. Yang J. Shen J. Reduced inhibition underlies early life LPS exposure induced-cognitive impairment: Prevention by environmental enrichment. Int. Immunopharmacol. 2022 108 108724 10.1016/j.intimp.2022.108724 35378446
    [Google Scholar]
  136. Ji M.H. Tang H. Luo D. Qiu L.L. Jia M. Yuan H.M. Feng S.W. Yang J.J. Environmental conditions differentially affect neurobehavioral outcomes in a mouse model of sepsis-associated encephalopathy. Oncotarget 2017 8 47 82376 82389 10.18632/oncotarget.19595 29137271
    [Google Scholar]
  137. Jiang S. Wang Y.Q. Tang Y. Lu X. Guo D. Environmen-tal enrichment protects against sepsis-associated encephalopa-thy-induced learning and memory deficits by enhancing the synthesis and release of vasopressin in the supraoptic nucle-us. J. Inflamm. Res. 2022 15 363 379 10.2147/JIR.S345108 35079222
    [Google Scholar]
  138. Korneev K.V. Mouse models of sepsis and septic shock. Mol. Biol. 2019 53 5 704 717 10.1134/S0026893319050108 31661479
    [Google Scholar]
  139. Qin M. Gao Y. Guo S. Lu X. Zhao Q. Ge Z. Zhu H. Li Y. Establishment and evaluation of animal models of sep-sis-associated encephalopathy. World J. Emerg. Med. 2023 14 5 349 353 10.5847/wjem.j.1920‑8642.2023.088 37908801
    [Google Scholar]
  140. Dejager L. Pinheiro I. Dejonckheere E. Libert C. Cecal ligation and puncture: the gold standard model for polymicro-bial sepsis? Trends Microbiol. 2011 19 4 198 208 10.1016/j.tim.2011.01.001 21296575
    [Google Scholar]
  141. Savi F.F. de Oliveira A. de Medeiros G.F. Bozza F.A. Michels M. Sharshar T. Dal-Pizzol F. Ritter C. What ani-mal models can tell us about long-term cognitive dysfunction following sepsis: A systematic review. Neurosci. Biobehav. Rev. 2021 124 386 404 10.1016/j.neubiorev.2020.12.005 33309906
    [Google Scholar]
  142. Granja M.G. Alves L.P. Leardini-Tristão M. Saul M.E. Bortoni L.C. de Moraes F.M. Ferreira E.C. de Moraes B.P.T. da Silva V.Z. dos Santos A.F.R. Silva A.R. Gon-çalves-de-Albuquerque, C.F.; Bambini-Junior, V.; Weyrich, A.S.; Rondina, M.T.; Zimmerman, G.A.; de Castro-Faria-Neto, H.C. Inflammatory, synaptic, motor, and behavioral al-terations induced by gestational sepsis on the offspring at dif-ferent stages of life. J. Neuroinflammation 2021 18 1 60 10.1186/s12974‑021‑02106‑1 33632243
    [Google Scholar]
  143. Lin L. Chen X. Zhou Q. Huang P. Jiang S. Wang H. Deng Y. Synaptic structure and alterations in the hippocam-pus in neonatal rats exposed to lipopolysaccharide. Neurosci. Lett. 2019 709 134364 10.1016/j.neulet.2019.134364 31288048
    [Google Scholar]
  144. Zhang S. Wang X. Ai S. Ouyang W. Le Y. Tong J. Sepsis-induced selective loss of NMDA receptors modulates hippocampal neuropathology in surviving septic mice. PLoS One 2017 12 11 e0188273 10.1371/journal.pone.0188273 29176858
    [Google Scholar]
  145. Weberpals M. Hermes M. Hermann S. Kummer M.P. Terwel D. Semmler A. Berger M. Schäfers M. Heneka M.T. NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J. Neurosci. 2009 29 45 14177 14184 10.1523/JNEUROSCI.3238‑09.2009 19906966
    [Google Scholar]
  146. Viviani B. Bartesaghi S. Gardoni F. Vezzani A. Behrens M.M. Bartfai T. Binaglia M. Corsini E. Di Luca M. Galli C.L. Marinovich M. Interleukin-1β enhances NMDA recep-tor-mediated intracellular calcium increase through activation of the Src family of kinases. J. Neurosci. 2003 23 25 8692 8700 10.1523/JNEUROSCI.23‑25‑08692.2003 14507968
    [Google Scholar]
  147. Spulber S. Mateos L. Oprica M. Cedazo-Minguez A. Bartfai T. Winblad B. Schultzberg M. Impaired long term memory consolidation in transgenic mice overexpressing the human soluble form of IL-1ra in the brain. J. Neuroimmunol. 2009 208 1-2 46 53 10.1016/j.jneuroim.2009.01.010 19211154
    [Google Scholar]
  148. Yasumura M. Yoshida T. Yamazaki M. Abe M. Natsu-me R. Kanno K. Uemura T. Takao K. Sakimura K. Kikusui T. Miyakawa T. Mishina M. IL1RAPL1 knockout mice show spine density decrease, learning deficiency, hyper-activity and reduced anxiety-like behaviours. Sci. Rep. 2014 4 1 6613 10.1038/srep06613 25312502
    [Google Scholar]
  149. Rossi S. Motta C. Musella A. Centonze D. The interplay between inflammatory cytokines and the endocannabinoid system in the regulation of synaptic transmission. Neuropharmacology 2015 96 Pt A 105 112 10.1016/j.neuropharm.2014.09.022 25268960
    [Google Scholar]
  150. Zhou Q. Lin L. Li H. Li Y. Liu N. Wang H. Jiang S. Li Q. Chen Z. Lin Y. Jin H. Deng Y. Intrahippocampal injection of IL‐1β upregulates Siah1‐mediated degradation of synaptophysin by activation of the ERK signaling in male rat. J. Neurosci. Res. 2023 101 6 930 951 10.1002/jnr.25170 36720002
    [Google Scholar]
  151. Vezzani A. Viviani B. Neuromodulatory properties of in-flammatory cytokines and their impact on neuronal excitabil-ity. Neuropharmacology 2015 96 Pt A 70 82 10.1016/j.neuropharm.2014.10.027 25445483
    [Google Scholar]
  152. Hisaoka-Nakashima K. Ohata K. Yoshimoto N. Tokuda S. Yoshii N. Nakamura Y. Wang D. Liu K. Wake H. Yoshida T. Ago Y. Hashimoto K. Nishibori M. Morioka N. High-mobility group box 1-mediated hippocampal micro-glial activation induces cognitive impairment in mice with neuropathic pain. Exp. Neurol. 2022 355 114146 10.1016/j.expneurol.2022.114146 35738416
    [Google Scholar]
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The Biological Changes of Synaptic Plasticity in the Pathological Process of Sepsis-associated Encephalopathy
Bentham Science Publishers ; https://doi.org/10.2174/1570159X23666241028105746
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  • Article Type:     Review Article
Keywords: sepsis-associated encephalopathy ; Sepsis ; inflammatory factors ; microglia ; synaptic plasticity ; neuroinflammation

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