Differential Effects of Sevoflurane Exposure on Long-Term Fear Memory in Neonatal and Adult Rats

Changsheng Li1, Sufang Liu2, Yixin Mei1, Qingyong Wang3, Xihua Lu1, Hongle Li4, Feng Tao2
1Department of Anesthesiology and Perioperative Medicine, Affiliated Cancer Hospital of Zhengzhou University, Zhengzhou, Henan, China
2Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75023, USA
3Department of Neurology, University of Chinese Academy of Sciences-Shenzhen Hospital, Shenzhen, China
4Department of Molecular Pathology, Affiliated Cancer Hospital of Zhengzhou University, 127 Dongming Road, Zhengzhou, Henan, 450008, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Xu T, Bo L, Wang J, Zhao Z, Xu Z, Deng X et al (2013) Risk factors for early postoperative cognitive dysfunction after non-coronary bypass surgery in Chinese population. J Cardiothorac Surg 8:204

Anand KJ, Soriano SG (2004) Anesthetic agents and the immature brain: are these toxic or therapeutic? Anesthesiology 101:527–530

Satomoto M, Satoh Y, Terui K, Miyao H, Takishima K, Ito M et al (2009) Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 110:628–637

Sun L (2010) Early childhood general anaesthesia exposure and neurocognitive development. Br J Anaesth 105(Suppl 1):i61–i68

Kang E, Jiang D, Ryu YK, Lim S, Kwak M, Gray CD et al (2017) Early postnatal exposure to isoflurane causes cognitive deficits and disrupts development of newborn hippocampal neurons via activation of the mTOR pathway. PLoS Biol. 15:e2001246

Tao F, Chen Q, Sato Y, Skinner J, Tang P, Johns RA (2015) Inhalational anesthetics disrupt postsynaptic density protein-95, Drosophila disc large tumor suppressor, and zonula occludens-1 domain protein interactions critical to action of several excitatory receptor channels related to anesthesia. Anesthesiology 122:776–786

Tao F, Johns RA (2008) Effect of disrupting N-methyl-d-aspartate receptor-postsynaptic density protein-95 interactions on the threshold for halothane anesthesia in mice. Anesthesiology 108:882–887

Tao F, Skinner J, Yang Y, Johns RA (2010) Effect of PSD-95/SAP90 and/or PSD-93/chapsyn-110 deficiency on the minimum alveolar anesthetic concentration of halothane in mice. Anesthesiology 112:1444–1451

Nikonenko I, Boda B, Steen S, Knott G, Welker E, Muller D (2008) PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling. J Cell Biol 183:1115–1127

Schiller MR, Ferraro F, Wang Y, Ma XM, McPherson CE, Sobota JA et al (2008) Autonomous functions for the Sec14p/spectrin-repeat region of Kalirin. Exp Cell Res 314:2674–2691

Ma XM, Wang Y, Ferraro F, Mains RE, Eipper BA (2008) Kalirin-7 is an essential component of both shaft and spine excitatory synapses in hippocampal interneurons. J Neurosci 28:711–724

Ma XM, Huang J, Wang Y, Eipper BA, Mains RE (2003) Kalirin, a multifunctional Rho guanine nucleotide exchange factor, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. J Neurosci 23:10593–10603

Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM et al (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640–656

Penzes P, Johnson RC, Alam MR, Kambampati V, Mains RE, Eipper BA (2000) An isoform of kalirin, a brain-specific GDP/GTP exchange factor, is enriched in the postsynaptic density fraction. J Biol Chem 275:6395–6403

Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, Kambampati V et al (2001) The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29:229–242

Lu J, Luo C, Bali KK, Xie RG, Mains RE, Eipper BA et al (2015) A role for Kalirin-7 in nociceptive sensitization via activity-dependent modulation of spinal synapses. Nat Commun 6:6820

Mandela P, Ma XM (2012) Kalirin, a key player in synapse formation, is implicated in human diseases. Neural Plast. 2012:728161

Puigdellivol M, Cherubini M, Brito V, Giralt A, Suelves N, Ballesteros J et al (2015) A role for Kalirin-7 in corticostriatal synaptic dysfunction in Huntington’s disease. Hum Mol Genet 24:7265–7285

Cahill ME, Jones KA, Rafalovich I, Xie Z, Barros CS, Muller U et al (2012) Control of interneuron dendritic growth through NRG1/erbB4-mediated kalirin-7 disinhibition. Mol Psychiatry 17(1):99–107

Jiao Y, Fan H, Wang K, Lu S (2019) Sevoflurane Impairs short-term memory by affecting PSD-95 and AMPA receptor in the hippocampus of a mouse model. Behav Neurol 2019:1068260

Nagura H, Ishikawa Y, Kobayashi K, Takao K, Tanaka T, Nishikawa K et al (2012) Impaired synaptic clustering of postsynaptic density proteins and altered signal transmission in hippocampal neurons, and disrupted learning behavior in PDZ1 and PDZ2 ligand binding-deficient PSD-95 knockin mice. Mol Brain 5:43

Ramage TM, Chang FL, Shih J, Alvi RS, Quitoriano GR, Rau V et al (2013) Distinct long-term neurocognitive outcomes after equipotent sevoflurane or isoflurane anaesthesia in immature rats. Br J Anaesth 110(Suppl 1):i39-46

Stratmann G, Alvi RS. Can minimum alveolar concentrations in immature rodents be a single number? Anesthesiology. 2011;115:1132–3; author's reply 3–5.

Kalenka A, Hinkelbein J, Feldmann RE, Jr., Kuschinsky W, Waschke KF, Maurer MH. The effects of sevoflurane anesthesia on rat brain proteins: a proteomic time-course analysis. Anesth Analg. 2007;104:1129–35, tables of contents.

Yoo SW, Bae M, Tovar YRLB, Haughey NJ (2017) Hippocampal encoding of interoceptive context during fear conditioning. Transl Psychiatry. 7:e991

Clem RL, Huganir RL (2010) Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330:1108–1112

Schaefer ML, Wang M, Perez PJ, Coca Peralta W, Xu J, Johns RA (2019) Nitric oxide donor prevents neonatal isoflurane-induced impairments in synaptic plasticity and memory. Anesthesiology 130:247–262

Folci A, Murru L, Vezzoli E, Ponzoni L, Gerosa L, Moretto E et al (2016) Myosin IXa binds AMPAR and regulates synaptic structure, LTP, and cognitive function. Front Mol Neurosci 9:1

Fiala JC, Harris KM (2001) Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8:1–16

Li C, Schaefer M, Gray C, Yang Y, Furmanski O, Liu S et al (2017) Sensitivity to isoflurane anesthesia increases in autism spectrum disorder Shank3(+/c) mutant mouse model. Neurotoxicol Teratol 60:69–74

Wang X, Cahill ME, Werner CT, Christoffel DJ, Golden SA, Xie Z et al (2013) Kalirin-7 mediates cocaine-induced AMPA receptor and spine plasticity, enabling incentive sensitization. J Neurosci 33:11012–11022

Li C, Yang Y, Liu S, Fang H, Zhang Y, Furmanski O et al (2014) Stress induces pain transition by potentiation of AMPA receptor phosphorylation. J Neurosci 34:13737–13746

Li C, Liu S, Xing Y, Tao F (2014) The role of hippocampal tau protein phosphorylation in isoflurane-induced cognitive dysfunction in transgenic APP695 mice. Anesth Analg 119:413–419

Callaway JK, Jones NC, Royse AG, Royse CF (2012) Sevoflurane anesthesia does not impair acquisition learning or memory in the Morris water maze in young adult and aged rats. Anesthesiology 117:1091–1101

Zhou L, Wang Z, Zhou H, Liu T, Lu F, Wang S et al (2015) Neonatal exposure to sevoflurane may not cause learning and memory deficits and behavioral abnormality in the childhood of Cynomolgus monkeys. Sci Rep 5:11145

Nakamura E, Kinoshita H, Feng GG, Hayashi H, Satomoto M, Sato M et al (2016) Sevoflurane inhalation accelerates the long-term memory consolidation via Small GTPase overexpression in the hippocampus of mice in adolescence. PLoS One. 11:e0163151

Almenrader N, Colucci P, De Castro V, Valeri D, Palmery M, Trezza V et al (2017) Effects of sevoflurane and clonidine on acid base status and long-term emotional and cognitive outcomes in spontaneously breathing rat pups. PLoS One. 12:e0173969

Flanigan TJ, Law CD, Ferguson SA (2021) Minimal effects from a single exposure to sevoflurane in adult male and female Sprague-Dawley rats. Neurotoxicol Teratol. 84:106955

Makaryus R, Lee H, Feng T, Park JH, Nedergaard M, Jacob Z et al (2015) Brain maturation in neonatal rodents is impeded by sevoflurane anesthesia. Anesthesiology 123:557–568

Colon E, Bittner EA, Kussman B, McCann ME, Soriano S, Borsook D (2017) Anesthesia, brain changes, and behavior: Insights from neural systems biology. Prog Neurobiol 153:121–160

Lin Y, Lei L, Ju LS, Xu N, Morey TE, Gravenstein N et al (2020) Neonatal exposure to sevoflurane expands the window of vulnerability to adverse effects of subsequent exposure to sevoflurane and alters hippocampal morphology via decitabine-sensitive mechanisms. Neurosci Lett. 735:135240

Lunardi N, Ori C, Erisir A, Jevtovic-Todorovic V (2010) General anesthesia causes long-lasting disturbances in the ultrastructural properties of developing synapses in young rats. Neurotox Res 17:179–188

Lu H, Liufu N, Dong Y, Xu G, Zhang Y, Shu L et al (2017) Sevoflurane acts on ubiquitination-proteasome pathway to reduce postsynaptic density 95 protein levels in young mice. Anesthesiology 127:961–975

Sommer JE, Budreck EC (2009) Kalirin-7: linking spine plasticity and behavior. J Neurosci 29:5367–5369

Fitzgerald PJ, Pinard CR, Camp MC, Feyder M, Sah A, Bergstrom HC et al (2015) Durable fear memories require PSD-95. Mol Psychiatry 20:901–912