Biomolecules & Therapeutics

  • 제23권3호
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  • Pages.251-260
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  • 2015
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  • 1976-9148(pISSN)
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  • 2005-4483(eISSN)
한국응용약물학회 (The Korean Society of Applied Pharmacology)
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Repeated Neonatal Propofol Administration Induces Sex-Dependent Long-Term Impairments on Spatial and Recognition Memory in Rats

  • Gonzales, Edson Luck T. (Department of Neuroscience, School of Medicine, and Neuroscience Research Center, SMART-IABS and KU Open Innovation Center, Konkuk University) ;
  • Yang, Sung Min (Department of Neuroscience, School of Medicine, and Neuroscience Research Center, SMART-IABS and KU Open Innovation Center, Konkuk University) ;
  • Choi, Chang Soon (Department of Neuroscience, School of Medicine, and Neuroscience Research Center, SMART-IABS and KU Open Innovation Center, Konkuk University) ;
  • Mabunga, Darine Froy N. (Department of Neuroscience, School of Medicine, and Neuroscience Research Center, SMART-IABS and KU Open Innovation Center, Konkuk University) ;
  • Kim, Hee Jin (Department of Pharmacy, Sahmyook University) ;
  • Cheong, Jae Hoon (Department of Pharmacy, Sahmyook University) ;
  • Ryu, Jong Hoon (Department of Oriental Pharmaceutical Science, Kyung Hee University) ;
  • Koo, Bon-Nyeo (Department of Anesthesiology and Pain Medicine, Anesthesia and Pain Research Institute, Yonsei University College of Medicine) ;
  • Shin, Chan Young (Department of Neuroscience, School of Medicine, and Neuroscience Research Center, SMART-IABS and KU Open Innovation Center, Konkuk University)
  • 투고 : 2014.10.17
  • 심사 : 2015.02.07
  • 발행 : 2015.05.01
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초록

Propofol is an anesthetic agent that gained wide use because of its fast induction of anesthesia and rapid recovery post-anesthesia. However, previous studies have reported immediate neurodegeneration and long-term impairment in spatial learning and memory from repeated neonatal propofol administration in animals. Yet, none of those studies has explored the sex-specific long-term physical changes and behavioral alterations such as social (sociability and social preference), emotional (anxiety), and other cognitive functions (spatial working, recognition, and avoidance memory) after neonatal propofol treatment. Seven-day-old Wistar-Kyoto (WKY) rats underwent repeated daily intraperitoneal injections of propofol or normal saline for 7 days. Starting fourth week of age and onwards, rats were subjected to behavior tests including open-field, elevated-plus-maze, Y-maze, 3-chamber social interaction, novel-object-recognition, passive-avoidance, and rotarod. Rats were sacrificed at 9 weeks and hippocampal protein expressions were analyzed by Western blot. Results revealed long-term body weight gain alterations in the growing rats and sex-specific impairments in spatial (female) and recognition (male) learning and memory paradigms. A markedly decreased expression of hippocampal NMDA receptor GluN1 subunit in female- and increased expression of AMPA GluR1 subunit protein expression in male rats were also found. Other aspects of behaviors such as locomotor activity and coordination, anxiety, sociability, social preference and avoidance learning and memory were not generally affected. These results suggest that neonatal repeated propofol administration disrupts normal growth and some aspects of neurodevelopment in rats in a sex-specific manner.

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참고문헌

  1. Anand, K. J. S., Phil, D. and Soriano, S. G. (2004) Anesthetic agents and the immature brain: Are these toxic or therapeutic? Anesthesiology 101, 527-530. https://doi.org/10.1097/00000542-200408000-00033
  2. Bevins, R. A. and Besheer, J. (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat. Protoc. 1, 1306-1311. https://doi.org/10.1038/nprot.2006.205
  3. Boon, W. C., Diepstraten, J., van der Burg, J., Jones, M. E., Simpson, E. R. and van den Buuse, M. (2005) Hippocampal NMDA receptor subunit expression and watermaze learning in estrogen deficient female mice. Brain Res. 140, 127-132. https://doi.org/10.1016/j.molbrainres.2005.07.004
  4. Brenhouse, H. C. and Andersen, S. L. (2011). Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci. Biobehav. Rev. 35, 1687-1703. https://doi.org/10.1016/j.neubiorev.2011.04.013
  5. Briner, A., Nikonenko, I., De Roo, M., Dayer, A., Muller, D. and Vutskits, L. (2011) Developmental Stage-dependent persistent impact of propofol anesthesia on dendritic spines in the rat medial prefrontal cortex. Anesthesiology 115, 282-293. https://doi.org/10.1097/ALN.0b013e318221fbbd
  6. Broadbent, N. J., Squire, L. R. and Clark, R. E. (2004) Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 101, 14515-14520. https://doi.org/10.1073/pnas.0406344101
  7. Cattano, D., Young, C., Straiko, M. M. and Olney, J. W. (2008) Subanesthetic doses of propofol induce neuroapoptosis in the infant mouse brain. Anesth. Analg 106, 1712-1714. https://doi.org/10.1213/ane.0b013e318172ba0a
  8. Chen, P. E., Errington, M. L., Kneussel, M., Chen, G., Annala, A. J., Rudhard, Y. H., Rast, G. F., Specht, C. G., Tigaret, C. M., Nassar, M. A., Morris, R. G., Bliss, T. V. and Schoepfer, R. (2009) Behavioral deficits and subregion-specific suppression of LTP in mice expressing a population of mutant NMDA receptors throughout the hippocampus. Learn. Mem. 16, 635-644. https://doi.org/10.1101/lm.1316909
  9. Cui, Y., Ling-Shan, G., Yi, L., Xing-Qi, W., Xue-Mei, Z. and Xiao-Xing, Y. (2011) Repeated administration of propofol upregulated the expression of c-Fos and cleaved-caspase-3 proteins in the developing mouse brain. Indian J. Pharmacol. 43, 648-651.
  10. D'Agata, V. and Cavallaro, S. (2003) Hippocampal gene expression profiles in passive avoidance conditioning. Eur. J. Neurosci. 18, 2835-2841. https://doi.org/10.1111/j.1460-9568.2003.03025.x
  11. Dobbing, J. and Sands, J. (1973) Quantitative growth and development of human brain. Arch. Dis. Child. 48, 757-767. https://doi.org/10.1136/adc.48.10.757
  12. Feng, C. S., Qiu, J. P., Ma, H. C. and Yue, Y. (2007) Effect of propofol on synaptic long-term potentiation in hippocampal slices of rats. Chi. J. Prev. Med. 87, 763-767.
  13. Flick, R. P., Katusic, S. K., Colligan, R. C., Wilder, R. T., Voigt, R. G., Olson, M. D., Sprung, J., Weaver, A. L., Schroeder, D. R. and Warner, D. O. (2011) Cognitive and behavioral outcomes after early exposure to anesthesia and surgery. Pediatrics 128, e1053-1061. https://doi.org/10.1542/peds.2011-0351
  14. Gao, J., Peng, S., Xiang, S., Huang, J. and Chen, P. (2014) Repeated exposure to propofol impairs spatial learning, inhibits LTP and reduces $CaMKII{\alpha}$ in young rats. Neurosci. Lett. 560, 62-66. https://doi.org/10.1016/j.neulet.2013.11.061
  15. Han, D., Tian, Y., Zhang, T., Ren, G. and Yang, Z. (2011) Nano-zinc oxide damages spatial cognition capability via over-enhanced long-term potentiation in hippocampus of Wistar rats. Int. J. Nanomedicine 6, 1453-1461.
  16. Hasselmo, M. E. (2006) The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710-715. https://doi.org/10.1016/j.conb.2006.09.002
  17. Hayashi, H., Dikkes, P. and Soriano, S. G. (2002) Repeated administration of ketamine may lead to neuronal degeneration in the developing rat brain. Pediatr. Anaesth. 12, 770-774. https://doi.org/10.1046/j.1460-9592.2002.00883.x
  18. Jevtovic-Todorovic, V., Hartman, R. E., Izumi, Y., Benshoff, N. D., Dikranian, K., Zorumski, C. F., Olney, J. W. and Wozniak, D. F. (2003) Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J. Neurosci 23, 876-882.
  19. Karen, T., Schlager, G. W., Bendix, I., Sifringer, M., Herrmann, R., Pantazis, C., Enot, D., Keller, M., Kerner, T. and Felderhoff-Mueser, U. (2013) Effect of propofol in the immature rat brain on short- and long-term neurodevelopmental outcome. PloS One 8, e64480. https://doi.org/10.1371/journal.pone.0064480
  20. Kikuchi, T., Wang, Y., Sato, K. and Okumura, F. (1998) In vivo effects of propofol on acetylcholine release from the frontal cortex, hippocampus and striatum studied by intracerebral microdialysis in freely moving rats. Br. J. Anaesth. 80, 644-648. https://doi.org/10.1093/bja/80.5.644
  21. Kim, K. C., Kim, P., Go, H. S., Choi, C. S., Yang, S.-I., Cheong, J. H., Shin, C. Y. and Ko, K. H. (2011). The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol. Lett. 201, 137-142. https://doi.org/10.1016/j.toxlet.2010.12.018
  22. Li, J., Xiong, M., Alhashem, H. M., Zhang, Y., Tilak, V., Patel, A., Siegel, A., Ye, J. H. and Bekker, A. (2014) Effects of prenatal propofol exposure on postnatal development in rats. Neurotixicol. Teratol. 43, 51-58. https://doi.org/10.1016/j.ntt.2014.03.006
  23. Lynch, M. A. (2004) Long-term potentiation and memory. Physiol. Rev. 84, 87-136. https://doi.org/10.1152/physrev.00014.2003
  24. Mallory, M. D., Baxter, A. L., Yanosky, D. J., Cravero, J. P. and Pediatric Sedation Research, C. (2011) Emergency physician-administered propofol sedation: a report on 25,433 sedations from the pediatric sedation research consortium. Ann Emerg Med 57, 462-468. https://doi.org/10.1016/j.annemergmed.2011.03.008
  25. Maurice, T., Phan, V. L., Noda, Y., Yamada, K., Privat, A. and Nabeshima, T. (1999) The attenuation of learning impairments induced after exposure to CO or trimethyltin in mice by sigma (${\sigma}$) receptor ligands involves both ${\sigma}1$ and ${\sigma}2$ sites. Br. J. Pharmacol. 127, 335-342. https://doi.org/10.1038/sj.bjp.0702553
  26. Milanovic, D., Popic, J., Pesic, V., Loncarevic-Vasiljkovic, N., Kanazir, S., Jevtovic-Todorovic, V. and Ruzdijic, S. (2010) Regional and temporal profiles of calpain and caspase-3 activities in postnatal rat brain following repeated propofol administration. Dev. Neurosci. 32, 288-301. https://doi.org/10.1159/000316970
  27. Morgan, D., Munireddy, S., Alamed, J., DeLeon, J., Diamond, D. M., Bickford, P., Hutton, M., Lewis, J., McGowan, E. and Gordon, M. N. (2008) Apparent behavioral benefits of tau overexpression in P301L tau transgenic mice. J. Alzheimers Dis. 15, 605-614. https://doi.org/10.3233/JAD-2008-15407
  28. Moy, S. S., Nadler, J. J., Perez, A., Barbaro, R. P., Johns, J. M., Magnuson, T. R., Piven, J. and Crawley, J. N. (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 3, 287-302. https://doi.org/10.1111/j.1601-1848.2004.00076.x
  29. Nakazawa, K., McHugh, T. J., Wilson, M. A. and Tonegawa, S. (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 5, 361-372. https://doi.org/10.1038/nrn1385
  30. Paoletti, P., Bellone, C. and Zhou, Q. (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 14, 383-400. https://doi.org/10.1038/nrn3504
  31. Pellow, S., Chopin, P., File, S. E. and Briley, M. (1985) Validation of open : closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167. https://doi.org/10.1016/0165-0270(85)90031-7
  32. Prut, L. and Belzung, C. (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33. https://doi.org/10.1016/S0014-2999(03)01272-X
  33. Sarter, M., Bodewitz, G. and Stephens, D. N. (1988) Attenuation of scopolamine-induced impairment of spontaneous alternation behaviour by antagonist but not inverse agonist and agonist ${\beta}$-carbolines. Psychopharmacology 94, 491-495. https://doi.org/10.1007/BF00212843
  34. Satomoto, M., Satoh, Y., Terui, K., Miyao, H., Takishima, K., Ito, M. and Imaki, J. (2009) Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 110, 628-637. https://doi.org/10.1097/ALN.0b013e3181974fa2
  35. Sun, L. (2010) Early childhood general anaesthesia exposure and neurocognitive development. Br. J. Anaesth. 105 Suppl 1, i61-68. https://doi.org/10.1093/bja/aeq302
  36. Uslaner, J. M., Parmentier-Batteur, S., Flick, R. B., Surles, N. O., Lam, J. S., McNaughton, C. H., Jacobson, M. A. and Hutson, P. H. (2009) Dose-dependent effect of CDPPB, the mGluR5 positive allosteric modulator, on recognition memory is associated with GluR1 and CREB phosphorylation in the prefrontal cortex and hippocampus. Neuropharmacology 57, 531-538. https://doi.org/10.1016/j.neuropharm.2009.07.022
  37. Wang, D., Noda, Y., Zhou, Y., Mouri, A., Mizoguchi, H., Nitta, A., Chen, W. and Nabeshima, T. (2007) The allosteric potentiation of nicotinic acetylcholine receptors by galantamine ameliorates the cognitive dysfunction in beta amyloid25-35 icv-injected mice: involvement of dopaminergic systems. Neuropsychopharmacol 32, 1261-1271. https://doi.org/10.1038/sj.npp.1301256
  38. Weigt, H. U., Georgieff, M., Beyer, C. and Fohr, K. J. (2002) Activation of neuronal N-methyl-D-aspartate receptor channels by lipid emulsions. Anesth. Analg. 94, 331-337. https://doi.org/10.1213/00000539-200202000-00018
  39. Wilder, R. T., Flick, R. P., Sprung, J., Katusic, S. K., Barbaresi, W. J., Mickelson, C., Gleich, S. J., Schroeder, D. R., Weaver, A. L. and Warner, D. O. (2009) Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 110, 796-804. https://doi.org/10.1097/01.anes.0000344728.34332.5d
  40. Xiong, M., Li, J., Alhashem, H. M., Tilak, V., Patel, A., Pisklakov, S., Siegel, A., Ye, J. H. and Bekker, A. (2014) Propofol exposure in pregnant rats induces neurotoxicity and persistent learning deficit in the offspring. Brain Sci. 4, 356-375. https://doi.org/10.3390/brainsci4020356
  41. Yan, J., Li, Y. R., Zhang, Y., Lu, Y. and Jiang, H. (2014) Repeated exposure to anesthetic ketamine can negatively impact neurodevelopment in infants: a prospective preliminary clinical study. J. Child. Neurol. 29, 1333-1338. https://doi.org/10.1177/0883073813517508
  42. Yon, J. H., Daniel-Johnson, J., Carter, L. B. and Jevtovic-Todorovic, V. (2005). Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience 135, 815-827. https://doi.org/10.1016/j.neuroscience.2005.03.064
  43. Yu, D., Jiang, Y., Gao, J., Liu, B. and Chen, P. (2013). Repeated exposure to propofol potentiates neuroapoptosis and long-term behavioral deficits in neonatal rats. Neurosci. Lett. 534, 41-46. https://doi.org/10.1016/j.neulet.2012.12.033

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  3. Etanercept, an inhibitor of TNF-a, prevents propofol-induced neurotoxicity in the developing brain vol.55, 2016, https://doi.org/10.1016/j.ijdevneu.2016.10.002
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  5. Review of preclinical studies on pediatric general anesthesia-induced developmental neurotoxicity vol.60, 2017, https://doi.org/10.1016/j.ntt.2016.11.005
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  17. Early Developmental Exposure to Repetitive Long Duration of Midazolam Sedation Causes Behavioral and Synaptic Alterations in a Rodent Model of Neurodevelopment vol.31, pp.1, 2015, https://doi.org/10.1097/ana.0000000000000541
  18. Using animal models to evaluate the functional consequences of anesthesia during early neurodevelopment vol.165, pp.None, 2015, https://doi.org/10.1016/j.nlm.2018.03.014
  19. Sex differences in neurodevelopmental abnormalities caused by early-life anaesthesia exposure: a narrative review vol.124, pp.3, 2015, https://doi.org/10.1016/j.bja.2019.12.032
  20. Neonatal anesthesia and dysregulation of the epigenome vol.105, pp.3, 2015, https://doi.org/10.1093/biolre/ioab136