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Markers of HPA-axis activity and nucleic acid damage from oxidation after electroconvulsive stimulations in rats

Published online by Cambridge University Press:  14 October 2019

Anders Jorgensen*
Affiliation:
Psychiatric Center Copenhagen (Rigshospitalet), Mental Health Services of the Capital Region of Denmark, Copenhagen, Denmark Laboratory of Neuropsychiatry, Psychiatric Center Copenhagen and Institute of Neuroscience and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Katrine Breitenstein
Affiliation:
Laboratory of Neuropsychiatry, Psychiatric Center Copenhagen and Institute of Neuroscience and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Otto Kalliokoski
Affiliation:
Department of Experimental Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Allan Weimann
Affiliation:
Laboratory of Clinical Pharmacology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark Department of Clinical Pharmacology, Copenhagen University Hospital Bispebjerg and Frederiksberg, Copenhagen, Denmark
Trine Henriksen
Affiliation:
Laboratory of Clinical Pharmacology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark Department of Clinical Pharmacology, Copenhagen University Hospital Bispebjerg and Frederiksberg, Copenhagen, Denmark
Henrik Enghusen Poulsen
Affiliation:
Laboratory of Clinical Pharmacology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark Department of Clinical Pharmacology, Copenhagen University Hospital Bispebjerg and Frederiksberg, Copenhagen, Denmark
Martin Balslev Jorgensen
Affiliation:
Psychiatric Center Copenhagen (Rigshospitalet), Mental Health Services of the Capital Region of Denmark, Copenhagen, Denmark Laboratory of Neuropsychiatry, Psychiatric Center Copenhagen and Institute of Neuroscience and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Gitta Wörtwein
Affiliation:
Laboratory of Neuropsychiatry, Psychiatric Center Copenhagen and Institute of Neuroscience and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
*
Author for correspondence: Anders Jorgensen, E-mail: [email protected]

Abstract

Objective:

Oxidative stress has been suggested to increase after electroconvulsive therapy (ECT), a treatment which continues to be the most effective for severe depression. Oxidative stress could potentially be mechanistically involved in both the therapeutic effects and side effects of ECT.

Methods:

We measured sensitive markers of systemic and central nervous system (CNS) oxidative stress on DNA and RNA (urinary 8-oxodG/8-oxoGuo, cerebrospinal fluid 8-oxoGuo, and brain oxoguanine glycosylase mRNA expression) in male rats subjected to electroconvulsive stimulations (ECS), an animal model of ECT. Due to the previous observations that link hypothalamic–pituitary–adrenal (HPA)-axis activity and age to DNA/RNA damage from oxidation, groups of young and middle-aged male animals were included, and markers of HPA-axis activity were measured.

Results:

ECS induced weight loss, increased corticosterone (only in middle-aged animals), and decreased cerebral glucocorticoid receptor mRNA expression, while largely leaving the markers of systemic and CNS DNA/RNA damage from oxidation unaltered.

Conclusion:

These results suggest that ECS is not associated with any lasting effects on oxidative stress on nucleic acids neither in young nor middle-aged rats.

Type
Original Article
Copyright
© Scandinavian College of Neuropsychopharmacology 2019 

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Footnotes

*

These authors contributed equally.

References

Barichello, T, Bonatto, F, Feier, G, Martins, MR, Moreira, JC, Dal-Pizzol, F, Izquierdo, I and Quevedo, J (2004) No evidence for oxidative damage in the hippocampus after acute and chronic electroshock in rats. Brain Research 1014, 177183.CrossRefGoogle ScholarPubMed
Barregard, L, Moller, P, Henriksen, T, Mistry, V, Koppen, G, Rossner, P Jr., Sram, RJ, Weimann, A, Poulsen, HE, Nataf, R and Andreoli, R (2013) Human and methodological sources of variability in the measurement of urinary 8-oxo-7, 8-dihydro-2’-deoxyguanosine. Antioxidants & Redox Signaling 18, 23772391.Google ScholarPubMed
Bodine, SC and Furlow, JD (2015) Glucocorticoids and skeletal muscle. Advances in Experimental Medicine and Biology 872, 145176.CrossRefGoogle ScholarPubMed
Bolwig, TG (2011) How does electroconvulsive therapy work? Theories on its mechanism. The Canadian Journal of Psychiatry 56, 1318.Google ScholarPubMed
Chen, F, Madsen, TM, Wegener, G and Nyengaard, JR (2009) Repeated electroconvulsive seizures increase the total number of synapses in adult male rat hippocampus. European Neuropsychopharmacology 19, 329338.CrossRefGoogle ScholarPubMed
Deng, XS, Tuo, J, Poulsen, HE and Loft, S (1998) Prevention of oxidative DNA damage in rats by brussels sprouts. Free Radical Research 28, 323333.Google ScholarPubMed
Dessens, FM, van Paassen, J, van Westerloo, DJ, van der Wee, NJ, van Vliet, IM and van Noorden, MS (2016) Electroconvulsive therapy in the intensive care unit for the treatment of catatonia: a case series and review of the literature. General Hospital Psychiatry 38, 3741.CrossRefGoogle ScholarPubMed
Epel, ES (2009) Psychological and metabolic stress: a recipe for accelerated cellular aging? Hormones(Athens) 8, 722.Google ScholarPubMed
Feier, G, Jornada, LK, Barichello, T, Vitali, AM, Bonatto, F, Moreira, JC, Dal-Pizzol, F and Quevedo, J (2006) Long lasting effects of electroconvulsive seizures on brain oxidative parameters. Neurochemical Research 31, 665670.Google ScholarPubMed
Flint, MS, Baum, A, Chambers, WH and Jenkins, FJ (2007) Induction of DNA damage, alteration of DNA repair and transcriptional activation by stress hormones. Psychoneuroendocrinology 32, 470479.Google ScholarPubMed
Gaffey, AE, Bergeman, CS, Clark, LA and Wirth, MM (2016) Aging and the HPA axis: stress and resilience in older adults. Neuroscience & Biobehavioral Reviews 68, 928945.Google ScholarPubMed
Hageman, I, Nielsen, M, Wortwein, G, Diemer, NH and Jorgensen, MB (2008) Electroconvulsive stimulations prevent stress-induced morphological changes in the hippocampus. Stress 11, 282289.Google ScholarPubMed
Hageman, I, Nielsen, M, Wortwein, G, Diemer, NH and Jorgensen, MB (2009) Electroconvulsive stimulations normalizes stress-induced changes in the glucocorticoid receptor and behaviour. Behavioural Brain Research 196, 7177.Google ScholarPubMed
Henriksen, T, Hillestrom, PR, Poulsen, HE and Weimann, A (2009) Automated method for the direct analysis of 8-oxo-guanosine and 8-oxo-2’-deoxyguanosine in human urine using ultraperformance liquid chromatography and tandem mass spectrometry. Free Radical Biology and Medicine 47, 629635.Google ScholarPubMed
Hjaeresen, ML, Hageman, I, Wortwein, G and Jorgensen, MB (2012) Time course and duration of changes in Kv7.2 and Kv11.1 mRNA expression in the hippocampus and piriform cortex following electroconvulsive stimulations. Brain Stimulation 5, 5560.Google ScholarPubMed
Joergensen, A, Broedbaek, K, Weimann, A, Semba, RD, Ferrucci, L, Joergensen, MB and Poulsen, HE (2011) Association between urinary excretion of cortisol and markers of oxidatively damaged DNA and RNA in humans. PLoSOne 6, e20795.CrossRefGoogle ScholarPubMed
Jorgensen, A, Broedbaek, K, Fink-Jensen, A, Knorr, U, Greisen Soendergaard, M, Henriksen, T, Weimann, A, Jepsen, P, Lykkesfeldt, J, Poulsen, HE and Jorgensen, MB (2013a) Increased systemic oxidatively generated DNA and RNA damage in schizophrenia. Psychiatry Research 209, 417423.Google Scholar
Jorgensen, A, Kalliokoski, O, Forsberg, K, Breitenstein, K, Weimann, A, Henriksen, T, Hau, J, Wörtwein, G, Poulsen, HE and Jorgensen, MB (2017) A chronic increase of corticosterone age-dependently reduces systemic DNA damage from oxidation in rats. Free Radical Biology and Medicine 104, 6474.CrossRefGoogle ScholarPubMed
Jorgensen, A, Krogh, J, Miskowiak, K, Bolwig, TG, Kessing, LV, Fink-Jensen, A, Nordentoft, M, Henriksen, T, Weimann, A, Poulsen, HE and Jorgensen, MB (2013b) Systemic oxidatively generated DNA/RNA damage in clinical depression: associations to symptom severity and response to electroconvulsive therapy. The Journal of Affective Disorders 149, 355362.Google ScholarPubMed
Jorgensen, A, Magnusson, P, Hanson, LG, Kirkegaard, T, Benveniste, H, Lee, H, Svarer, C, Mikkelsen, JD, Fink-Jensen, A, Knudsen, GM and Paulson, OB (2016) Regional brain volumes, diffusivity, and metabolite changes after electroconvulsive therapy for severe depression. Acta Psychiatrica Scandinavica 133, 154164.CrossRefGoogle ScholarPubMed
Jorgensen, A, Maigaard, K, Wortwein, G, Hageman, I, Henriksen, T, Weimann, A, Møller, P, Loft, S, Hau, J, Poulsen, HE and Jorgensen, MB (2013c) Chronic restraint stress in rats causes sustained increase in urinary corticosterone excretion without affecting cerebral or systemic oxidatively generated DNA/RNA damage. Progress in Neuro-Psychopharmacology & Biological Psychiatry 40, 3037.Google ScholarPubMed
Jornada, LK, Feier, G, Barichello, T, Vitali, AM, Reinke, A, Gavioli, EC, Dal-Pizzol, F and Quevedo, J (2007) Effects of maintenance electroshock on the oxidative damage parameters in the rat brain. Neurochemical Research 32, 389394.Google ScholarPubMed
Joshi, SH, Espinoza, RT, Pirnia, T, Shi, J, Wang, Y, Ayers, B, Leaver, A, Woods, RP and Narr, KL (2016) Structural plasticity of the hippocampus and amygdala induced by electroconvulsive therapy in major depression. Biological Psychiatry 79, 282292.Google ScholarPubMed
Madsen, TM, Treschow, A, Bengzon, J, Bolwig, TG, Lindvall, O and Tingstrom, A (2000) Increased neurogenesis in a model of electroconvulsive therapy. Biological Psychiatry 47, 10431049.CrossRefGoogle Scholar
Mahat, MY, Fakrudeen Ali Ahamed, N, Chandrasekaran, S, Rajagopal, S, Narayanan, S and Surendran, N (2012) An improved method of transcutaneous cisterna magna puncture for cerebrospinal fluid sampling in rats. The Journal of Neuroscience Methods 211, 272279.CrossRefGoogle ScholarPubMed
Moller, P, Lohr, M, Folkmann, JK, Mikkelsen, L and Loft, S (2010) Aging and oxidatively damaged nuclear DNA in animal organs. Free Radical Biology and Medicine 48, 12751285.Google ScholarPubMed
Nater, UM, Hoppmann, CA and Scott, SB (2013) Diurnal profiles of salivary cortisol and alpha-amylase change across the adult lifespan: evidence from repeated daily life assessments. Psychoneuroendocrinology 38, 31673171.Google ScholarPubMed
Nielsen, RM, Olsen, KS, Lauritsen, AO and Boesen, HC (2014) Electroconvulsive therapy as a treatment for protracted refractory delirium in the intensive care unit -- five cases and a review. Journal of Critical Care 29, 881.e1886.e6.CrossRefGoogle ScholarPubMed
Osler, M, Rozing, MP, Christensen, GT, Andersen, PK and Jorgensen, MB (2018) Electroconvulsive therapy and risk of dementia in patients with affective disorders: a cohort study. The Lancet Psychiatry 5, 348356.Google ScholarPubMed
Poulsen, HE, Nadal, LL, Broedbaek, K, Nielsen, PE and Weimann, A (2014) Detection and interpretation of 8-oxodG and 8-oxoGua in urine, plasma and cerebrospinal fluid. Biochimica et Biophysica Acta 1840, 801808.CrossRefGoogle ScholarPubMed
Rasmussen, ST, Andersen, JT, Nielsen, TK, Cejvanovic, V, Petersen, KM, Henriksen, T, Weimann, A, Lykkesfeldt, J and Poulsen, HE (2016) Simvastatin and oxidative stress in humans: a randomized, double-blinded, placebo-controlled clinical trial. Redox Biology 9, 3238.Google ScholarPubMed
Semkovska, M and McLoughlin, DM (2010) Objective cognitive performance associated with electroconvulsive therapy for depression: a systematic review and meta-analysis. Biological Psychiatry 68, 568577.Google ScholarPubMed
Semkovska, M and McLoughlin, DM (2013) Measuring retrograde autobiographical amnesia following electroconvulsive therapy: historical perspective and current issues. The Journal of ECT 29, 127133.CrossRefGoogle ScholarPubMed
Suijk, DLS, Dols, A, van Exel, E, Stek, ML, Veltman, E, Bouckaert, F, Sienaert, P and Rhebergen, D (2018) Salivary cortisol as predictor for depression characteristics and remission in electroconvulsive therapy in older persons. The World Journal of Biological Psychiatry Feb 21, 18.CrossRefGoogle Scholar
UK_ECT_Review_Group (2003) Efficacy and safety of electroconvulsive therapy in depressive disorders: a systematic review and meta-analysis. Lancet 361, 799808.CrossRefGoogle Scholar
Zupan, G, Pilipovic, K, Hrelja, A and Peternel, S (2008) Oxidative stress parameters in different rat brain structures after electroconvulsive shock-induced seizures. Progress in Neuro-Psychopharmacology & Biological Psychiatry 32, 771777.Google ScholarPubMed