Effect of different charges of modified electroconvulsive seizure on the cognitive behavior in stressed rats: Effects of GluR1 phosphorylation and CaMKIIα activity

Zhang,Fan; Huang,Guihua; Zhu,Xianlin

doi:10.3892/etm.2018.7022

Effect of different charges of modified electroconvulsive seizure on the cognitive behavior in stressed rats: Effects of GluR1 phosphorylation and CaMKIIα activity

Authors:
- Fan Zhang
- Guihua Huang
- Xianlin Zhu
View Affiliations

Affiliations: Department of Anesthesiology, The People's Hospital of Jianyang City, Chengdu, Sichuan 610000, P.R. China, Department of Anesthesiology, The First People's Hospital of Zunyi, Zunyi, Guizhou 563000, P.R. China, Department of Anesthesiology, The Central Hospital of Enshi Autonomous Prefecture, Enshi, Hubei 445000, P.R. China
Published online on: November 28, 2018 https://doi.org/10.3892/etm.2018.7022
Pages: 748-758
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Electroconvulsive therapy (ECT) is an efﬁcient therapy for major depression and modern ECT requires anesthesia to enhance safety. However, the commonly used anesthetic, propofol, may weaken the treatment efﬁcacy. A recent study confirmed that ketamine rapidly reduced the symptoms of depression in affected patients. A previous study found that electroconvulsive seizure (ECS), the animal model for ECT, under anesthesia of low‑dose ketamine combined with propofol could enhance the antidepressant efficacy and improve the cognitive performance. The present study aimed to investigate the responses to different charges (0, 60, 120, 180 or 240 mC) of ECS under compound anesthetics, ketamine combined with propofol, in stressed rats and the underlying mechanisms to aid in optimization of treatment regimens. The results indicated that ECS exhibited an improved antidepressant effects at 120 mC compared with 60 mC, however, no significant differences in antidepressant effects were identified among the 120, 180 and 240 mC groups. Furthermore, rats subjected to ECS at 120 mC exhibited the best cognitive performance. The phosphorylation levels of calcium/calmodulin‑dependent protein kinase IIα (CaMKIIα) at Thr286, glutamate receptor 1 (GluR1) at Ser831 and cAMP‑response element‑binding protein (CREB) at the Ser133 were higher in the 120‑mC group compared with all other groups. These results indicated that the ECS at medium intensity (120 mC) with administration of compound anesthetics may exert an improved therapeutic effect on depression compared with other intensities (0, 60, 180 and 240 mC). The results also suggested that the improvement in cognitive function in stressed rats may be attributed to the phosphorylation of CaMKIIα (Thr286), GluR1 (Ser831) and CREB (Ser133).

View Figures

View References

1	Han J, Wang LU, Bian H, Zhou X and Ruan C: Effects of paroxetine on spatial memory function and protein kinase C expression in a rat model of depression. Exp Ther Med. 10:1489–1492. 2015. View Article : Google Scholar : PubMed/NCBI
2	Pittenger C and Duman RS: Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology. 33:88–109. 2008. View Article : Google Scholar : PubMed/NCBI
3	Pagnin D, de Queiroz V, Pini S and Cassano GB: Efficacy of ECT in depression: A meta-analytic review. J ECT. 20:13–20. 2004. View Article : Google Scholar : PubMed/NCBI
4	Lisanby SH: Electroconvulsive therapy for depression. N Engl J Med. 357:1939–1945. 2007. View Article : Google Scholar : PubMed/NCBI
5	Patel AS, Gorst-Unsworth C, Venn RM, Kelley K and Jacob Y: Anesthesia and electroconvulsive therapy: A retrospective study comparing etomidate and propofol. J ECT. 22:179–183. 2006. View Article : Google Scholar : PubMed/NCBI
6	Luo J, Min S, Wei K, Cao J, Wang B, Li P, Dong J and Liu Y: Propofol prevents electroconvulsive-shock-induced memory impairment through regulation of hippocampal synaptic plasticity in a rat model of depression. Neuropsychiatr Dis Treat. 10:1847–1859. 2014.PubMed/NCBI
7	Zhu X, Hao X, Luo J, Min S, Xie F and Zhang F: Propofol inhibits inflammatory cytokine-mediated glutamate uptake dysfunction to alleviate learning/memory impairment in depressed rats undergoing electroconvulsive shock. Brain Res. 1595:101–109. 2015. View Article : Google Scholar : PubMed/NCBI
8	Rampton A, Griffin R, Durcan J and Stuart C: Propofol and electroconvulsive therapy. Lancet. 331:296–297. 1988. View Article : Google Scholar
9	Warnell RL, Swartz CM and Thomson A: Propofol interruption of ECT seizure to reduce side-effects: A pilot study. Psychiatry Res. 175:184–185. 2010. View Article : Google Scholar : PubMed/NCBI
10	Naughton M, Clarke G, O'Leary OF, Cryan JF and Dinan TG: A review of ketamine in affective disorders: Current evidence of clinical efficacy, limitations of use and pre-clinical evidence on proposed mechanisms of action. J Affect Disord. 156:24–35. 2014. View Article : Google Scholar : PubMed/NCBI
11	White PF, Way WL and Trevor AJ: Ketamine-its pharmacology and therapeutic uses. Anesthesiology. 56:119–136. 1982. View Article : Google Scholar : PubMed/NCBI
12	Kranaster L, Kammerer-Ciernioch J, Hoyer C and Sartorius A: Clinically favourable effects of ketamine as an anaesthetic for electroconvulsive therapy: A retrospective study. Eur Arch Psychiatry Clin Neurosci. 261:575–582. 2011. View Article : Google Scholar : PubMed/NCBI
13	Okamoto N, Nakai T, Sakamoto K, Nagafusa Y, Higuchi T and Nishikawa T: Rapid antidepressant effect of ketamine anesthesia during electroconvulsive therapy of treatment-resistant depression: Comparing ketamine and propofol anesthesia. J ECT. 26:223–227. 2010. View Article : Google Scholar : PubMed/NCBI
14	Zarate CA, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA, Charney DS and Manji HK: A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry. 63:856–864. 2006. View Article : Google Scholar : PubMed/NCBI
15	Corlett PR, Honey GD, Aitken MR, Dickinson A, Shanks DR, Absalom AR, Lee M, Pomarol-Clotet E, Murray GK, McKenna PJ, et al: Frontal responses during learning predict vulnerability to the psychotogenic effects of ketamine: Linking cognition, brain activity and psychosis. Arch Gen Psychiatry. 63:611–621. 2006. View Article : Google Scholar : PubMed/NCBI
16	Bowdle AT, Radant AD, Cowley DS, Kharasch ED, Strassman RJ and Roy-Byrne PP: Psychedelic effects of ketamine in healthy volunteers relationship to steady-state plasma concentrations. J Am Soc Anesthesiologists. 88:82–88. 1998.
17	Chen J, Peng LH, Luo J, Liu L, Lv F, Li P, Ao L, Hao XC and Min S: Effects of low-dose ketamine combined with propofol on phosphorylation of AMPA receptor GluR1 subunit and GABAA receptor in hippocampus of stressed rats receiving electroconvulsive shock. J ECT. 31:50–56. 2015. View Article : Google Scholar : PubMed/NCBI
18	Andrade C, Kurinji S, Sudha S and Chandra JS: Effects of pulse amplitude, pulse frequency and stimulus duration on seizure threshold: A laboratory investigation. J ECT. 18:144–148. 2002. View Article : Google Scholar : PubMed/NCBI
19	Xu Y, Li X, Wang X, Yao J and Zhuang S: miR-34a deficiency in APP/PS1 mice promotes cognitive function by increasing synaptic plasticity via AMPA and NMDA receptors. Neurosci Lett. 670:94–104. 2018. View Article : Google Scholar : PubMed/NCBI
20	Treccani G, Kristian GDJ, Wegener G and Müller HK: Differential expression of postsynaptic NMDA and AMPA receptor subunits in the hippocampus and prefrontal cortex of the flinders sensitive line rat model of depression. Synapse. 70:471–474. 2016. View Article : Google Scholar : PubMed/NCBI
21	Maeng S, Zarate CA Jr, Du J, Schloesser RJ, McCammon J, Chen G and Manji HK: Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol Psychiatry. 63:349–352. 2008. View Article : Google Scholar : PubMed/NCBI
22	Greger IH, Ziff EB and Penn AC: Molecular determinants of AMPA receptor subunit assembly. Trends Neurosci. 30:407–416. 2007. View Article : Google Scholar : PubMed/NCBI
23	Nordgren M, Karlsson T, Svensson M, Koczy J, Josephson A, Olson L, Tingström A and Brené S: Orchestrated regulation of Nogo receptors, LOTUS, AMPA receptors and BDNF in an ECT model suggests opening and closure of a window of synaptic plasticity. PLoS One. 8:e787782013. View Article : Google Scholar : PubMed/NCBI
24	Keifer J and Zheng Z: AMPA receptor trafficking and learning. Eur J Neurosci. 32:269–277. 2010. View Article : Google Scholar : PubMed/NCBI
25	Bracey JM, Kurz JE, Low B and Churn SB: Prolonged seizure activity leads to increased protein kinase A activation in the rat pilocarpine model of status epilepticus. Brain Res. 1283:167–176. 2009. View Article : Google Scholar : PubMed/NCBI
26	Coultrap SJ, Zaegel V and Bayer KU: CaMKII isoforms differ in their specific requirements for regulation by nitric oxide. FEBS Lett. 588:4672–4676. 2014. View Article : Google Scholar : PubMed/NCBI
27	Ren L, Zhang F, Min S, Hao X, Qin P and Zhu X: Propofol ameliorates electroconvulsive shock-induced learning and memory impairment by regulation of synaptic metaplasticity via autophosphorylation of CaMKIIa at Thr 305 in stressed rats. Psychiatry Res. 240:123–130. 2016. View Article : Google Scholar : PubMed/NCBI
28	Banasr M, Valentine GW, Li XY, Gourley SL, Taylor JR and Duman RS: Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol Psychiatry. 62:496–504. 2007. View Article : Google Scholar : PubMed/NCBI
29	Karolina P, Barbara B and Grazyna B: Utility of the chronic unpredictable mild stress model in research on new antidepressants. Curr Issue Pharm Med Sci. 27:97–101. 2014. View Article : Google Scholar
30	Luo KR, Hong CJ, Liou YJ, Hou SJ, Huang YH and Tsai SJ: Differential regulation of neurotrophin S100B and BDNF in two rat models of depression. Prog Neuropsychopharmacol Biol Psychiatry. 34:1433–1439. 2010. View Article : Google Scholar : PubMed/NCBI
31	Xie F, Min S, Liu L, Peng L, Hao X and Zhu X: Advanced age enhances the sepsis-induced up-regulation of the γ- and α7-nicotinic acetylcholine receptors in different parts of the skeletal muscles. Arch Gerontology Geriatr. 65:1–8. 2016. View Article : Google Scholar
32	Segi-Nishida E, Warner-Schmidt JL and Duman RS: Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. Proc Natl Acad Sci USA. 105:11352–11357. 2008. View Article : Google Scholar : PubMed/NCBI
33	Luo J, Min S, Wei K, Zhang J and Liu Y: Propofol interacts with stimulus intensities of electroconvulsive shock to regulate behavior and hippocampal BDNF in a rat model of depression. Psychiatry Res. 198:300–306. 2012. View Article : Google Scholar : PubMed/NCBI
34	Ding L, Zhang X, Guo H, Yuan J, Li S, Hu W, Golden T and Wu N: The functional study of a chinese herbal compounded antidepressant medicine-jie yu chu fan capsule on chronic unpredictable mild stress mouse model. PLoS One. 10:e01334052015. View Article : Google Scholar : PubMed/NCBI
35	Cao XZ, Ma H, Wang JK, Liu F, Wu BY, Tian AY, Wang LL and Tan WF: Postoperative cognitive deficits and neuroinflammation in the hippocampus triggered by surgical trauma are exacerbated in aged rats. Prog Neuropsychopharmacology Biol Psychiatry. 34:1426–1432. 2010. View Article : Google Scholar
36	Liao WT, Xiao XY, Zhu Y and Zhou SP: The effect of celastrol on learning and memory in diabetic rats after sevoflurane inhalation. Arch Med Sci. 14:370–380. 2018. View Article : Google Scholar : PubMed/NCBI
37	Tianzhu Z, Shihai Y and Juan D: Antidepressant-like effects of cordycepin in a mice model of chronic unpredictable mild stress. Evid Based Complement Alternat Med. 2014:4385062014. View Article : Google Scholar : PubMed/NCBI
38	Willner P, Towell A, Sampson D, Sophokleous S and Muscat R: Reduction of sucrose preference by chronic unpredictable mild stress and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl). 93:358–364. 1987. View Article : Google Scholar : PubMed/NCBI
39	Willner P: Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology (Berl). 134:319–329. 1997. View Article : Google Scholar : PubMed/NCBI
40	Xinxing W, Wei L, Lei W, Rui Z, Baoying J and Lingjia Q: A neuroendocrine mechanism of co-morbidity of depression-like behavior and myocardial injury in rats. PLoS One. 9:e884272014. View Article : Google Scholar : PubMed/NCBI
41	Garcia LS, Comim CM, Valvassori SS, Réus GZ, Stertz L, Kapczinski F, Gavioli EC and Quevedo J: Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats. Prog Neuropsychopharmacol Biol Psychiatry. 33:450–455. 2009. View Article : Google Scholar : PubMed/NCBI
42	Caligiuri MP and Ellwanger J: Motor and cognitive aspects of motor retardation in depression. J Affect Disord. 57:83–93. 2000. View Article : Google Scholar : PubMed/NCBI
43	Frey R, Heiden A, Scharfetter J, Schreinzer D, Blasbichler T, Tauscher J, Felleiter P and Kasper S: Inverse relation between stimulus intensity and seizure duration: Implications for ECT procedure. J ECT. 17:102–108. 2001. View Article : Google Scholar : PubMed/NCBI
44	Wang X, Yang Y, Zhou X, Qu Q, Ou C, Liu L and Zhou S: Propofol pretreatment increases antidepressant-like effects induced by acute administration of ketamine in rats receiving forced swimming test. Psychiatry Res. 185:248–253. 2011. View Article : Google Scholar : PubMed/NCBI
45	Alves HN, da Silva AL, Olsson IA, Orden JM and Antunes LM: Anesthesia with intraperitoneal propofol, medetomidine, and fentanyl in rats. J Am Assoc Lab Anim Sci. 49:454–459. 2010.PubMed/NCBI
46	Taşkara E, Gör A, Kutlu O, Karagüzel E, Topbaş M and Şenel AC: Does propofol prevent testicular ischemia-reperfusion injury due to torsion in the long term? Pediatr Surg Int. 27:1003–1007. 2011. View Article : Google Scholar : PubMed/NCBI
47	Kushikata T, Sawada M, Niwa H, Kudo T, Kudo M, Tonosaki M and 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. 30:437–443. 2016. View Article : Google Scholar : PubMed/NCBI
48	Nikiforuk A and Popik P: Ketamine prevents stress-induced cognitive inflexibility in rats. Psychoneuroendocrinology. 40:119–122. 2014. View Article : Google Scholar : PubMed/NCBI
49	Sackeim HA, Devanand DP and Prudic J: Stimulus intensity, seizure threshold and seizure duration: Impact on the efficacy and safety of electroconvulsive therapy. Psychiatr Clin North Am. 14:803–843. 1991. View Article : Google Scholar : PubMed/NCBI
50	Carter SD, Mifsud KR and Reul JM: Distinct epigenetic and gene expression changes in rat hippocampal neurons after Morris water maze training. Front Behav Neurosci. 9:1562015. View Article : Google Scholar : PubMed/NCBI
51	Zots MA, Ivashkina OI, Ivanova AA and Anokhin KV: Formation of spatial and nonspatial memory in different condensed versions of short-term learning in morris water maze. Bull Exp Biol Med. 156:602–604. 2014. View Article : Google Scholar : PubMed/NCBI
52	Erdogan Kayhan G, Yucel A, Colak YZ, Ozgul U, Yologlu S, Karlıdag R and Ersoy MO: Ketofol (mixture of ketamine and propofol) administration in electroconvulsive therapy. Anaesth Intensive Care. 40:305–310. 2012.PubMed/NCBI
53	Wang D, Wang X, Liu X, Jiang L, Yang G, Shi X, Zhang C and Piao F: Inhibition of miR-219 alleviates arsenic-induced learning and memory impairments and synaptic damage through up-regulating CaMKII in the hippocampus. Neurochem Res. 43:948–958. 2018. View Article : Google Scholar : PubMed/NCBI
54	Matsuzaki K, Miyazaki K, Sakai S, Yawo H, Nakata N, Moriguchi S, Fukunaga K, Yokosuka A, Sashida Y, Mimaki Y, et al: Nobiletin, a citrus flavonoid with neurotrophic action, augments protein kinase A-mediated phosphorylation of the AMPA receptor subunit, GluR1 and the postsynaptic receptor response to glutamate in murine hippocampus. Eur J Pharmacol. 578:194–200. 2008. View Article : Google Scholar : PubMed/NCBI
55	Lee HK, Barbarosie M, Kameyama K, Bear MF and Huganir RL: Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature. 405:955–959. 2000. View Article : Google Scholar : PubMed/NCBI
56	Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, Petralia RS, et al: Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 112:631–643. 2003. View Article : Google Scholar : PubMed/NCBI
57	Singleton MW, Holbert WH II, Lee AT, Bracey JM and Churn SB: Modulation of CaM kinase II activity is coincident with induction of status epilepticus in the rat pilocarpine model. Epilepsia. 46:1389–1400. 2005. View Article : Google Scholar : PubMed/NCBI
58	Wu LJ, Ren M, Wang H, Kim SS, Cao X and Zhuo M: Neurabin contributes to hippocampal long-term potentiation and contextual fear memory. PLoS One. 3:e14072008. View Article : Google Scholar : PubMed/NCBI
59	Fumagalli F, Pasini M, Sartorius A, Scherer R, Racagni G, Riva MA and Gass P: Repeated electroconvulsive shock (ECS) alters the phosphorylation of glutamate receptor subunits in the rat hippocampus. Int J Neuropsychopharmacol. 13:1255–1260. 2010. View Article : Google Scholar : PubMed/NCBI
60	Tanis KQ, Duman RS and Newton SS: CREB binding and activity in brain: Regional specificity and induction by electroconvulsive seizure. Biol Psychiatry. 63:710–720. 2008. View Article : Google Scholar : PubMed/NCBI
61	Carlezon WA Jr, Duman RS and Nestler EJ: The many faces of CREB. Trends Neurosci. 28:436–445. 2005. View Article : Google Scholar : PubMed/NCBI
62	Qiu S and Currás-Collazo MC: Histopathological and molecular changes produced by hippocampal microinjection of domoic acid. Neurotoxicol Teratology. 28:354–362. 2006. View Article : Google Scholar