Advertisement

Journal of Molecular Neuroscience

, Volume 64, Issue 3, pp 346–351 | Cite as

Effect of Sevoflurane Anesthesia on Brain Is Mediated by lncRNA HOTAIR

  • Jian-yue Wang
  • Yong Feng
  • Yan-hong Fu
  • Guang-li Liu
Article

Abstract

Postoperative cognitive dysfunction in elderly patients has been related to neurodegenerative disorders and mortality. Sevoflurane anesthesia has been implicated in both postoperative cognitive dysfunction and neurotoxicity. Given the advantages of using inhaled anesthetics like sevoflurane, it is important to understand how their usage results in neurotoxicity and subsequently devise ways to circumvent or attenuate the anesthetic-mediated induction in neurotoxicity. Long noncoding RNAs (LncRNAs) are a group of > 200 bp long RNAs and show specific spatiotemporal expression profiles. Several recent reports suggest that lncRNAs are involved in responses of the central nervous system (CNS) following acute injuries. However, their role in sevoflurane anesthesia-mediated cognitive dysfunction has not been studied. RNA immunoprecipitation (RIP) combined with qRT-PCR detection of six different lncRNAs showed that the HOTAIR lncRNAs were significantly more bound to both Sin3A and coREST, both corepressors of the RE-1 silencing transcription factor, within rat hippocampus following sevoflurane anesthesia compared with sham. Sevoflurane inhalation resulted in significant inhibition of brain-derived neurotrophic factor (BDNF) and cognitive impairment. Treatment with a combination of siRNAs targeting HOTAIR rescued BDNF expression and improved cognitive responses. Taken together, our results suggest that sevoflurane-mediated brain function impairment is at least in part mediated by the HOTAIR lncRNA.

Keywords

Long noncoding RNA HOTAIR Sevoflurane Cognitive impairment 

Notes

Compliance with Ethical Standards

All procedures were approved by the Local Ethics Committee at Binzhou People’s Hospital.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Abe Y, Kikuchi A, Kobayashi S, Wakusawa K, Tanaka S, Inui T, Kunishima S, Kure S, Haginoya K (2014) Xq26.1-26.2 gain identified on array comparative genomic hybridization in bilateral periventricular nodular heterotopia with overlying polymicrogyria. Dev Med Child Neurol 56(12):1221–1224.  https://doi.org/10.1111/dmcn.12553 CrossRefPubMedGoogle Scholar
  2. Barbash S, Simchovitz A, Buchman AS, Bennett DA, Shifman S, Soreq HL (2017) Neuronal-expressed microRNA-targeted pseudogenes compete with coding genes in the human brain. Transl Psychiatry 7(8):e1199.  https://doi.org/10.1038/tp.2017.163 CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bekker AY, Weeks EJ (2003) Cognitive function after anaesthesia in the elderly. Best Pract Res Clin Anaesthesiol 17(2):259–272.  https://doi.org/10.1016/S1521-6896(03)00005-3 CrossRefPubMedGoogle Scholar
  4. Bittner EA, Yue Y, Xie Z (2011) Brief review: anesthetic neurotoxicity in the elderly, cognitive dysfunction and Alzheimer’s disease. Can J Anaesth = J canadien d'anesthésie 58(2):216–223.  https://doi.org/10.1007/s12630-010-9418-x CrossRefGoogle Scholar
  5. Bond AM, Vangompel MJ, Sametsky EA, Clark MF, Savage JC, Disterhoft JF, Kohtz JD (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12(8):1020–1027.  https://doi.org/10.1038/nn.2371 CrossRefPubMedCentralPubMedGoogle Scholar
  6. Brosnan H, Bickler PE (2013) Xenon neurotoxicity in rat hippocampal slice cultures is similar to isoflurane and sevoflurane. Anesthesiology 119(2):335–344.  https://doi.org/10.1097/ALN.0b013e31829417f0 CrossRefPubMedGoogle Scholar
  7. Bussemakers MJ, Van BA, Verhaegh GW, Smit FP, Karthaus HF, Schalken JA, Debruyne FM, Ru N, Isaacs WB (1999) DD3: a new prostate-specific gene, highly overexpressed in prostate cancer. Cancer Res 59:5975PubMedGoogle Scholar
  8. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25(18):1915–1927.  https://doi.org/10.1101/gad.17446611 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Castrén E (2004) Neurotrophic effects of antidepressant drugs. Curr Opin Pharmacol 4(1):58–64.  https://doi.org/10.1016/j.coph.2003.10.004 CrossRefPubMedGoogle Scholar
  10. Erden V, Erkalp K, Yangin Z, Delatioglu H, Kiroglu S, Ortakuz S, Ozdemir B (2011) The effect of labor on sevoflurane requirements during cesarean delivery. Int J Obstet Anesth 20(1):17–21.  https://doi.org/10.1016/j.ijoa.2010.08.008 CrossRefPubMedGoogle Scholar
  11. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368(6467):147–150.  https://doi.org/10.1038/368147a0 CrossRefPubMedGoogle Scholar
  12. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464(7291):1071–1076.  https://doi.org/10.1038/nature08975 CrossRefPubMedCentralPubMedGoogle Scholar
  13. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477(7364):295–300.  https://doi.org/10.1038/nature10398 CrossRefPubMedCentralPubMedGoogle Scholar
  14. Hall J, Thomas KL, Everitt BJ (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3(6):533–535.  https://doi.org/10.1038/75698 CrossRefPubMedGoogle Scholar
  15. Huang EJ, Reichardt LF (2001) NEUROTROPHINS: roles in neuronal development and Function1. Annu Rev Neurosci 24(1):677–736.  https://doi.org/10.1146/annurev.neuro.24.1.677 CrossRefPubMedCentralPubMedGoogle Scholar
  16. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmannbroz D, Khalil AM, Zuk O, Amit I, Rabani M (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142(3):409–419.  https://doi.org/10.1016/j.cell.2010.06.040 CrossRefPubMedCentralPubMedGoogle Scholar
  17. Iacoangeli A, Lin Y, Morley EJ, Muslimov IA, Bianchi R, Reilly J, Weedon J, Diallo R, Böcker W, Tiedge H (2004) BC200 RNA in invasive and preinvasive breast cancer. Carcinogenesis 25(11):2125–2133.  https://doi.org/10.1093/carcin/bgh228 CrossRefPubMedGoogle Scholar
  18. Iversen LL, Glowinski J (1966) Regional differences in the rate of turnover of norepinephrine in the rat brain. Nature 210(5040):1006–1008.  https://doi.org/10.1038/2101006a0 CrossRefPubMedGoogle Scholar
  19. Johnson R (2012) Long non-coding RNAs in Huntington’s disease neurodegeneration. Neurobiol Dis 46(2):245–254.  https://doi.org/10.1016/j.nbd.2011.12.006 CrossRefPubMedGoogle Scholar
  20. Kesslak JP, So V, Choi J, Cotman CW, Gomezpinilla F (1998) Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav Neurosci 112(4):1012–1019.  https://doi.org/10.1037/0735-7044.112.4.1012 CrossRefPubMedGoogle Scholar
  21. Kobayashi K, Takemori K, Sakamoto A (2007) Circadian gene expression is suppressed during sevoflurane anesthesia and the suppression persists after awakening. Brain Res 1185:1–7.  https://doi.org/10.1016/j.brainres.2007.09.011 CrossRefPubMedGoogle Scholar
  22. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92(19):8856–8860.  https://doi.org/10.1073/pnas.92.19.8856 CrossRefPubMedCentralPubMedGoogle Scholar
  23. Liang G, Ward C, Peng J, Zhao Y, Huang B, Wei H (2010) Isoflurane causes greater neurodegeneration than an equivalent exposure of sevoflurane in the developing brain of neonatal mice. Anesthesiology 112(6):1325–1334.  https://doi.org/10.1097/ALN.0b013e3181d94da5 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Lopez Gil ML, Brimacombe J, Clar B (1999) Sevoflurane versus propofol for induction and maintenance of anaesthesia with the laryngeal mask airway in children. Paediatr Anaesth 9(6):485–490.  https://doi.org/10.1046/j.1460-9592.1999.00404.x CrossRefPubMedGoogle Scholar
  25. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD (1990) NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5(4):501–509.  https://doi.org/10.1016/0896-6273(90)90089-X CrossRefPubMedGoogle Scholar
  26. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T (2000) Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20:7116PubMedGoogle Scholar
  27. Moller JT, Cluitmans P, Rasmussen LS, Houx P, Rasmussen H, Canet J, Rabbitt P, Jolles J, Larsen K, Hanning CD (1998) Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet 351:857CrossRefPubMedGoogle Scholar
  28. Nagano T, Fraser P (2011) No-nonsense functions for long noncoding RNAs. Cell 145(2):178–181.  https://doi.org/10.1016/j.cell.2011.03.014 CrossRefPubMedGoogle Scholar
  29. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Fergusonsmith AC, Feil R, Fraser P (2008) The air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322(5908):1717–1720.  https://doi.org/10.1126/science.1163802 CrossRefPubMedGoogle Scholar
  30. Pandey RR, Kanduri C (2011) Transcriptional and posttranscriptional programming by long noncoding RNAs. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  31. Perez DS, Hoage TR, Pritchett JR, Ducharmesmith AL, Halling ML, Ganapathiraju SC, Streng PS, Smith DI (2008) Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 17(5):642–655.  https://doi.org/10.1093/hmg/ddm336 CrossRefPubMedGoogle Scholar
  32. Petrovics G, Zhang W, Makarem M, Street JP, Connelly R, Sun L, Sesterhenn IA, Srikantan V, Moul JW, Srivastava S (2004) Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 23(2):605–611.  https://doi.org/10.1038/sj.onc.1207069 CrossRefPubMedGoogle Scholar
  33. Qureshi IA, Mehler MF (2011) Non-coding RNA networks underlying cognitive disorders across the lifespan. Trends Mol Med 17(6):337–346.  https://doi.org/10.1016/j.molmed.2011.02.002 CrossRefPubMedCentralPubMedGoogle Scholar
  34. Rasmussen LS, Johnson T, Kuipers HM, Kristensen D, Siersma VD, Vila P, Jolles J, Papaioannou A, Abildstrom H, Silverstein JH (2003) Does anaesthesia cause postoperative cognitive dysfunction? A randomised study of regional versus general anaesthesia in 438 elderly patients. Acta Anaesthesiol Scand 47(3):260–266.  https://doi.org/10.1034/j.1399-6576.2003.00057.x CrossRefPubMedGoogle Scholar
  35. Ray PS, Wang J, Qu Y, Sim MS, Shamonki J, Bagaria SP, Ye X, Liu B, Elashoff D, Hoon DS (2010) FOXC1 is a potential prognostic biomarker with functional significance in basal-like breast cancer. Cancer Res 70(10):3870–3876.  https://doi.org/10.1158/0008-5472.CAN-09-4120 CrossRefPubMedGoogle Scholar
  36. Salta E (2012) Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol 11(2):189–200.  https://doi.org/10.1016/S1474-4422(11)70286-1 CrossRefPubMedGoogle Scholar
  37. Satomoto M, Satoh Y, Terui K, Miyao H, Takishima K, Ito M, Imaki J (2009) Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 110(3):628–637.  https://doi.org/10.1097/ALN.0b013e3181974fa2 CrossRefPubMedGoogle Scholar
  38. Sauvageau M, Goff LA, Lodato S, Bonev B, Groff AF, Gerhardinger C, Sanchez-Gomez DB, Hacisuleyman E, Li E, Spence M, Liapis SC, Mallard W, Morse M, Swerdel MR, D'Ecclessis MF, Moore JC, Lai V, Gong G, Yancopoulos GD, Frendewey D, Kellis M, Hart RP, Valenzuela DM, Arlotta P, Rinn JL (2013) Multiple knockout mouse models reveal lincRNAs are required for life and brain development. elife 2:e01749CrossRefPubMedCentralPubMedGoogle Scholar
  39. Silbert B, Evered L, Scott DA, Maruff P (2011) Anesthesiology must play a greater role in patients with Alzheimer’s disease. Anesth Analg 112(5):1242–1245.  https://doi.org/10.1213/ANE.0b013e3182147f5b CrossRefPubMedGoogle Scholar
  40. Srikantan V, Zou Z, Petrovics G, Xu L, Augustus M, Davis L, Livezey JR, Connell T, Sesterhenn IA, Yoshino K (2000) PCGEM1, a prostate-specific gene, is overexpressed in prostate cancer. Proc Natl Acad Sci U S A 97(22):12216–12221.  https://doi.org/10.1073/pnas.97.22.12216 CrossRefPubMedCentralPubMedGoogle Scholar
  41. Steinmetz J, Christensen KB, Lund T, Lohse N, Rasmussen LS, Group, I (2009) Long-term consequences of postoperative cognitive dysfunction. Anesthesiology 110(3):548–555.  https://doi.org/10.1097/ALN.0b013e318195b569 CrossRefPubMedGoogle Scholar
  42. Stiegler MP, Tung A (2014) Cognitive processes in anesthesiology decision making. Anesthesiology 120(1):204–217.  https://doi.org/10.1097/ALN.0000000000000073 CrossRefPubMedGoogle Scholar
  43. Xiao H, Liu B, Chen Y, Zhang J (2016) Learning, memory and synaptic plasticity in hippocampus in rats exposed to sevoflurane. Int J Dev Neurosci 48:38.  https://doi.org/10.1016/j.ijdevneu.2015.11.001 CrossRefPubMedGoogle Scholar
  44. Xiong WX, Zhou GX, Wang B, Xue ZG, Wang L, Sun HC, Ge SJ (2013) Impaired spatial learning and memory after sevoflurane-nitrous oxide anesthesia in aged rats is associated with down-regulated cAMP/CREB signaling. PLoS One 8(11):e79408.  https://doi.org/10.1371/journal.pone.0079408 CrossRefPubMedCentralPubMedGoogle Scholar
  45. Yee BK, Zhu SW, Mohammed AH, Feldon J (2007) Levels of neurotrophic factors in the hippocampus and amygdala correlate with anxiety- and fear-related behaviour in C57BL6 mice. J Neural Transm 114(4):431–444.  https://doi.org/10.1007/s00702-006-0548-9 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of AnesthesiologyBinzhou People’s HospitalBinzhouChina

Personalised recommendations