nach oben

Erschienen in:

22.07.2019 | Original Article

Phospholipase C-related inactive protein type-1 deficiency affects anesthetic electroencephalogram activity induced by propofol and etomidate in mice

verfasst von: Tomonori Furukawa, Yoshikazu Nikaido, Shuji Shimoyama, Yoshiki Ogata, Tetsuya Kushikata, Kazuyoshi Hirota, Takashi Kanematsu, Masato Hirata, Shinya Ueno

Erschienen in: Journal of Anesthesia | Ausgabe 4/2019

Einloggen, um Zugang zu erhalten

Abstract

Purpose

The general anesthetics propofol and etomidate mainly exert their anesthetic actions via GABA A receptor (GABA_A-R). The GABA_A-R activity is influenced by phospholipase C-related inactive protein type-1 (PRIP-1), which is related to trafficking and subcellular localization of GABA_A-R. PRIP-1 deficiency attenuates the behavioral reactions to propofol but not etomidate. However, the effect of these anesthetics and of PRIP-1 deficiency on brain activity of CNS are still unclear. In this study, we examined the effects of propofol and etomidate on the electroencephalogram (EEG).

Methods

The cortical EEG activity was recorded in wild-type (WT) and PRIP-1 knockout (PRIP-1 KO) mice. All recorded EEG data were offline analyzed, and the power spectral density and 95% spectral edge frequency of EEG signals were compared between genotypes before and after injections of anesthetics.

Results

PRIP-1 deficiency induced increases in EEG absolute powers, but did not markedly change the relative spectral powers during waking and sleep states in the absence of anesthesia. Propofol administration induced increases in low-frequency relative EEG activity and decreases in SEF95 values in WT but not in PRIP-1 KO mice. Following etomidate injection, low-frequency EEG power was increased in both genotype groups. At high frequency, the relative power in PRIP-1 KO mice was smaller than that in WT mice.

Conclusions

The lack of PRIP-1 disrupted the EEG power distribution, but did not affect the depth of anesthesia after etomidate administration. Our analyses suggest that PRIP-1 is differentially involved in anesthetic EEG activity with the regulation of GABA_A-R activity.

Nur mit Berechtigung zugänglich

Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G. Cortical firing and sleep homeostasis. Neuron. 2009;63(6):865–78.CrossRefPubMedPubMedCentral

Purdon PL, Pierce ET, Mukamel EA, Prerau MJ, Walsh JL, Wong KF, Salazar-Gomez AF, Harrell PG, Sampson AL, Cimenser A, Ching S, Kopell NJ, Tavares-Stoeckel C, Habeeb K, Merhar R, Brown EN. Electroencephalogram signatures of loss and recovery of consciousness from propofol. Proc Natl Acad Sci USA. 2013;110(12):E1142–E1151151.CrossRefPubMed

Wang K, Steyn-Ross ML, Steyn-Ross DA, Wilson MT, Sleigh JW. EEG slow-wave coherence changes in propofol-induced general anesthesia: experiment and theory. Front Syst Neurosci. 2014;8:215.CrossRefPubMedPubMedCentral

Kuizenga K, Wierda JM, Kalkman CJ. Biphasic EEG changes in relation to loss of consciousness during induction with thiopental, propofol, etomidate, midazolam or sevoflurane. Br J Anaesth. 2001;86(3):354–60.CrossRefPubMed

Murphy M, Bruno MA, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant JF, Phillips C, Massimini M, Laureys S, Tononi G, Boly M. Propofol anesthesia and sleep: a high-density EEG study. Sleep. 2011;34(3):283–91.CrossRefPubMedPubMedCentral

Gabor G, Judit T, Zsolt I. Comparison of propofol and etomidate regarding impact on seizure threshold during electroconvulsive therapy in patients with schizophrenia. Neuropsychopharmacol Hung. 2007;9(3):125–30.PubMed

Tan HL, Lee CY. Comparison between the effects of propofol and etomidate on motor and electroencephalogram seizure duration during electroconvulsive therapy. Anaesth Intensive Care. 2009;37(5):807–14.CrossRefPubMed

Drexler B, Jurd R, Rudolph U, Antkowiak B. Distinct actions of etomidate and propofol at beta3-containing gamma-aminobutyric acid type A receptors. Neuropharmacology. 2009;57(4):446–55.CrossRefPubMed

Kim MG, Park SW, Kim JH, Lee J, Kae SH, Jang HJ, Koh DH, Choi MH. Etomidate versus propofol sedation for complex upper endoscopic procedures: a prospective double-blinded randomized controlled trial. Gastrointest Endosc. 2017;86(3):452–61.CrossRefPubMed

10.

Jurd R, Arras M, Lambert S, Drexler B, Siegwart R, Crestani F, Zaugg M, Vogt KE, Ledermann B, Antkowiak B, Rudolph U. General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit. FASEB J. 2003;17(2):250–2.CrossRefPubMed

11.

Feng HJ, Macdonald RL. Multiple actions of propofol on alphabetagamma and alphabetadelta GABA_A receptors. Mol Pharmacol. 2004;66(6):1517–24.CrossRefPubMed

12.

Sanchis-Segura C, Cline B, Jurd R, Rudolph U, Spanagel R. Etomidate and propofol-hyposensitive GABA_A receptor beta3(N265M) mice show little changes in acute alcohol sensitivity but enhanced tolerance and withdrawal. Neurosci Lett. 2007;416(3):275–8.CrossRefPubMed

13.

Hill-Venning C, Belelli D, Peters JA, Lambert JJ. Subunit-dependent interaction of the general anaesthetic etomidate with the gamma-aminobutyric acid type A receptor. Br J Pharmacol. 1997;120(5):749–56.CrossRefPubMedPubMedCentral

14.

Belelli D, Muntoni AL, Merrywest SD, Gentet LJ, Casula A, Callachan H, Madau P, Gemmell DK, Hamilton NM, Lambert JJ, Sillar KT, Peters JA. The in vitro and in vivo enantioselectivity of etomidate implicates the GABA_A receptor in general anaesthesia. Neuropharmacology. 2003;45(1):57–71.CrossRefPubMed

15.

Belelli D, Peden DR, Rosahl TW, Wafford KA, Lambert JJ. Extrasynaptic GABA_A receptors of thalamocortical neurons: a molecular target for hypnotics. J Neurosci. 2005;25(50):11513–20.CrossRefPubMed

16.

Cirone J, Rosahl TW, Reynolds DS, Newman RJ, O'Meara GF, Hutson PH, Wafford KA. Gamma-aminobutyric acid type A receptor beta 2 subunit mediates the hypothermic effect of etomidate in mice. Anesthesiology. 2004;100(6):1438–45.CrossRefPubMed

17.

Haenschel C, Baldeweg T, Croft RJ, Whittington M, Gruzelier J. Gamma and beta frequency oscillations in response to novel auditory stimuli: a comparison of human electroencephalogram (EEG) data with in vitro models. Proc Natl Acad Sci USA. 2000;97(13):7645–50.CrossRefPubMed

18.

Terunuma M, Jang IS, Ha SH, Kittler JT, Kanematsu T, Jovanovic JN, Nakayama KI, Akaike N, Ryu SH, Moss SJ, Hirata M. GABA_A receptor phospho-dependent modulation is regulated by phospholipase C-related inactive protein type 1, a novel protein phosphatase 1 anchoring protein. J Neurosci. 2004;24(32):7074–84.CrossRefPubMed

19.

Kanematsu T, Yasunaga A, Mizoguchi Y, Kuratani A, Kittler JT, Jovanovic JN, Takenaka K, Nakayama KI, Fukami K, Takenawa T, Moss SJ, Nabekura J, Hirata M. Modulation of GABA(A) receptor phosphorylation and membrane trafficking by phospholipase C-related inactive protein/protein phosphatase 1 and 2A signaling complex underlying brain-derived neurotrophic factor-dependent regulation of GABAergic inhibition. J Biol Chem. 2006;281(31):22180–9.CrossRefPubMed

20.

Kanematsu T, Mizokami A, Watanabe K, Hirata M. Regulation of GABA(A)-receptor surface expression with special reference to the involvement of GABARAP (GABA(A) receptor-associated protein) and PRIP (phospholipase C-related, but catalytically inactive protein). J Pharmacol Sci. 2007;104(4):285–92.CrossRefPubMed

21.

Yanagihori S, Terunuma M, Koyano K, Kanematsu T, Ho Ryu S, Hirata M. Protein phosphatase regulation by PRIP, a PLC-related catalytically inactive protein–implications in the phospho-modulation of the GABAA receptor. Adv Enzyme Regul. 2006;46:203–22.CrossRefPubMed

22.

Migita K, Tomiyama M, Yamada J, Fukuzawa M, Kanematsu T, Hirata M, Ueno S. Phenotypes of pain behavior in phospholipase C-related but catalytically inactive protein type 1 knockout mice. Mol Pain. 2011;7:79.CrossRefPubMedPubMedCentral

23.

Zhu G, Yoshida S, Migita K, Yamada J, Mori F, Tomiyama M, Wakabayashi K, Kanematsu T, Hirata M, Kaneko S, Ueno S, Okada M. Dysfunction of extrasynaptic GABAergic transmission in phospholipase C-related, but catalytically inactive protein 1 knockout mice is associated with an epilepsy phenotype. J Pharmacol Exp Ther. 2012;340(3):520–8.CrossRefPubMed

24.

Nikaido Y, Furukawa T, Shimoyama S, Yamada J, Migita K, Koga K, Kushikata T, Hirota K, Kanematsu T, Hirata M, Ueno S. Propofol anesthesia is reduced in phospholipase c-related inactive protein type-1 knockout mice. J Pharmacol Exp Ther. 2017;361(3):367–74.CrossRefPubMed

25.

Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell. 1999;98(4):437–51.CrossRef

26.

Guan Z, Vgontzas AN, Bixler EO, Fang J. Sleep is increased by weight gain and decreased by weight loss in mice. Sleep. 2008;31(5):627–33.CrossRefPubMedPubMedCentral

27.

Kushikata T, Sawada M, Niwa H, Kudo T, Kudo M, Tonosaki M, Hirota K. Ketamine and propofol have opposite effects on postanesthetic sleep architecture in rats: relevance to the endogenous sleep-wakefulness substances orexin and melanin-concentrating hormone. J Anesth. 2016;30(3):437–43.CrossRefPubMed

28.

Rudolph U, Mohler H. Analysis of GABA_A receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol. 2004;44:475–98.CrossRefPubMed

29.

Ferguson C, Hardy SL, Werner DF, Hileman SM, Delorey TM, Homanics GE. New insight into the role of the beta3 subunit of the GABA_A-R in development, behavior, body weight regulation, and anesthesia revealed by conditional gene knockout. BMC Neurosci. 2007;8:85.CrossRefPubMedPubMedCentral

30.

DeLorey TM, Handforth A, Anagnostaras SG, Homanics GE, Minassian BA, Asatourian A, Fanselow MS, Delgado-Escueta A, Ellison GD, Olsen RW. Mice lacking the beta3 subunit of the GABA_A receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J Neurosci. 1998;18(20):8505–14.CrossRefPubMed

31.

Liljelund P, Handforth A, Homanics GE, Olsen RW. GABA_A receptor beta3 subunit gene-deficient heterozygous mice show parent-of-origin and gender-related differences in beta3 subunit levels, EEG, and behavior. Brain Res Dev Brain Res. 2005;157(2):150–61.CrossRefPubMed

32.

Krasowski MD, Rick CE, Harrison NL, Firestone LL, Homanics GE. A deficit of functional GABA(A) receptors in neurons of beta 3 subunit knockout mice. Neurosci Lett. 1998;240(2):81–4.CrossRefPubMedPubMedCentral

33.

Wisor JP, DeLorey TM, Homanics GE, Edgar DM. Sleep states and sleep electroencephalographic spectral power in mice lacking the beta 3 subunit of the GABA(A) receptor. Brain Res. 2002;955(1–2):221–8.CrossRefPubMed

34.

Sidorov MS, Deck GM, Dolatshahi M, Thibert RL, Bird LM, Chu CJ, Philpot BD. Delta rhythmicity is a reliable EEG biomarker in Angelman syndrome: a parallel mouse and human analysis. J Neurodev Disord. 2017;9:17.CrossRefPubMedPubMedCentral

35.

Kanematsu T, Jang IS, Yamaguchi T, Nagahama H, Yoshimura K, Hidaka K, Matsuda M, Takeuchi H, Misumi Y, Nakayama K, Yamamoto T, Akaike N, Hirata M. Role of the PLC-related, catalytically inactive protein p130 in GABA(A) receptor function. EMBO J. 2002;21(5):1004–111.CrossRefPubMedPubMedCentral

36.

Flores FJ, Hartnack KE, Fath AB, Kim SE, Wilson MA, Brown EN, Purdon PL. Thalamocortical synchronization during induction and emergence from propofol-induced unconsciousness. Proc Natl Acad Sci USA. 2017;114(32):E6660–E666868.CrossRefPubMed

37.

Lambert S, Arras M, Vogt KE, Rudolph U. Isoflurane-induced surgical tolerance mediated only in part by beta3-containing GABA(A) receptors. Eur J Pharmacol. 2005;516(1):23–7.CrossRefPubMed

38.

Liao M, Sonner JM, Jurd R, Rudolph U, Borghese CM, Harris RA, Laster MJ, Eger EI, 2nd. Beta3-containing gamma-aminobutyric acid A receptors are not major targets for the amnesic and immobilizing actions of isoflurane. Anesth Analg. 2005;101(2):412–8 (table of contents).

39.

Reynolds DS, Rosahl TW, Cirone J, O'Meara GF, Haythornthwaite A, Newman RJ, Myers J, Sur C, Howell O, Rutter AR, Atack J, Macaulay AJ, Hadingham KL, Hutson PH, Belelli D, Lambert JJ, Dawson GR, McKernan R, Whiting PJ, Wafford KA. Sedation and anesthesia mediated by distinct GABA(A) receptor isoforms. J Neurosci. 2003;23(24):8608–17.CrossRefPubMed

40.

Drexler B, Roether CL, Jurd R, Rudolph U, Antkowiak B. Opposing actions of etomidate on cortical theta oscillations are mediated by different gamma-aminobutyric acid type A receptor subtypes. Anesthesiology. 2005;102(2):346–52.CrossRefPubMed

41.

Butovas S, Rudolph U, Jurd R, Schwarz C, Antkowiak B. Activity patterns in the prefrontal cortex and hippocampus during and after awakening from etomidate anesthesia. Anesthesiology. 2010;113(1):48–57.CrossRefPubMed

42.

Uji A, Matsuda M, Kukita T, Maeda K, Kanematsu T, Hirata M. Molecules interacting with PRIP-2, a novel Ins(1,4,5)P3 binding protein type 2: comparison with PRIP-1. Life Sci. 2002;72(4–5):443–53.CrossRefPubMed

43.

Brunig I, Scotti E, Sidler C, Fritschy JM. Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol. 2002;443(1):43–55.CrossRefPubMed

44.

Sieghart W, Sperk G. Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem. 2002;2(8):795–816.CrossRefPubMed

45.

Wang H, Luo M, Li C, Wang G. Propofol post-conditioning induced long-term neuroprotection and reduced internalization of AMPAR GluR2 subunit in a rat model of focal cerebral ischemia/reperfusion. J Neurochem. 2011;119(1):210–9.CrossRefPubMed

46.

Hales TG, Lambert JJ. The actions of propofol on inhibitory amino acid receptors of bovine adrenomedullary chromaffin cells and rodent central neurones. Br J Pharmacol. 1991;104(3):619–28.CrossRefPubMedPubMedCentral

47.

Kingston S, Mao L, Yang L, Arora A, Fibuch EE, Wang JQ. Propofol inhibits phosphorylation of N-methyl-d-aspartate receptor NR1 subunits in neurons. Anesthesiology. 2006;104(4):763–9.CrossRefPubMed

48.

Qiu Q, Sun L, Wang XM, Lo ACY, Wong KL, Gu P, Wong SCS, Cheung CW. Propofol produces preventive analgesia via GluN2B-containing NMDA Receptor/ERK1/2 Signaling Pathway in a rat model of inflammatory pain. Mol Pain. 2017;13:1744806917737462.CrossRefPubMedPubMedCentral

49.

Chen D, Qi X, Zhuang R, Cao J, Xu Y, Huang X, Li Y. Prenatal propofol exposure downregulates NMDA receptor expression and causes cognitive and emotional disorders in rats. Eur J Pharmacol. 2019;843:268–76.CrossRefPubMed

50.

Lin CR, Cheng JT, Lin FC, Chou AK, Lee TC, Chen JT, Yang LC. Effect of thiopental, propofol, and etomidate on vincristine toxicity in PC12 cells. Cell Biol Toxicol. 2002;18(1):63–70.CrossRefPubMed

51.

Kassem LA, Gamal El-Din MM, Yassin NA. Mechanisms of vincristine-induced neurotoxicity: Possible reversal by erythropoietin. Drug Discov Ther. 2011;5(3):136–43.CrossRefPubMed

52.

Putzke C, Hanley PJ, Schlichthörl G, Preisig-Müller R, Rinné S, Anetseder M, Eckenhoff R, Berkowitz C, Vassiliou T, Wulf H, Eberhart L. Differential effects of volatile and intravenous anesthetics on the activity of human TASK-1. Am J Physiol Cell Physiol. 2007;293(4):C1319–C13261326.CrossRefPubMed

53.

Lazarenko RM, Willcox SC, Shu S, Berg AP, Jevtovic-Todorovic V, Talley EM, Chen X, Bayliss DA. Motoneuronal TASK channels contribute to immobilizing effects of inhalational general anesthetics. J Neurosci. 2010;30(22):7691–704.CrossRefPubMedPubMedCentral

54.

Franks NP. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci. 2008;9(5):370–86.CrossRefPubMed

55.

Sugiyama G, Takeuchi H, Kanematsu T, Gao J, Matsuda M, Hirata M. Phospholipase C-related but catalytically inactive protein, PRIP as a scaffolding protein for phospho-regulation. Adv Biol Regul. 2013;53(3):331–40.CrossRefPubMed

56.

Shortal BP, Reitz SL, Aggarwal A, Meng QC, McKinstry-Wu AR, Kelz MB, Proekt A. Development and validation of brain target controlled infusion of propofol in mice. PLoS ONE. 2018;13(4):e0194949.CrossRefPubMedPubMedCentral

57.

Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G. GABA_A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neurosci. 2000;101(4):815–50.CrossRef

Titel: Phospholipase C-related inactive protein type-1 deficiency affects anesthetic electroencephalogram activity induced by propofol and etomidate in mice
verfasst von: Tomonori Furukawa
Yoshikazu Nikaido
Shuji Shimoyama
Yoshiki Ogata
Tetsuya Kushikata
Kazuyoshi Hirota
Takashi Kanematsu
Masato Hirata
Shinya Ueno
Publikationsdatum: 22.07.2019
Verlag: Springer Japan
Erschienen in: Journal of Anesthesia / Ausgabe 4/2019
Print ISSN: 0913-8668
Elektronische ISSN: 1438-8359
DOI: https://doi.org/10.1007/s00540-019-02663-z

Update AINS

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

hier abonnieren

Springer Medizin

Phospholipase C-related inactive protein type-1 deficiency affects anesthetic electroencephalogram activity induced by propofol and etomidate in mice