An acetylcholinesterase inhibitor,donepezil,increases anxiety and cortisol levels in adult zebrafish

Abreu MS Giacomini A Kalueff AV , et al. (2016) The smell of “anxiety”: Behavioral modulation by experimental anosmia in zebrafish. Physiol Behav 157: 67–71.

Alachkar A Łażewska D Kieć-Kononowicz K , et al. (2017) The histamine H3 receptor antagonist E159 reverses memory deficits induced by dizocilpine in passive avoidance and novel object recognition paradigm in rats. Front Pharmacol 8: 709.

Ambrogio F Martella LA Odetti P , et al. (2019) Behavioral disturbances in dementia and beyond: Time for a new conceptual frame? Int J Mol Sci 20: 3647.

Avdesh A Chen M Martin-Iverson MT , et al. (2012) Regular care and maintenance of a zebrafish (Danio rerio) laboratory: An introduction. J Vis Exp e4196. DOI: 10.3791/4196.

Ben-Azu B Nwoke EE Aderibigbe AO , et al. (2019) Possible neuroprotective mechanisms of action involved in the neurobehavioral property of naringin in mice. Biomed Pharmacother 109: 536–546.

Bertuzzi M Ampatzis K (2018) Spinal cholinergic interneurons differentially control motoneuron excitability and alter the locomotor network operational range. Sci Rep 8: 1988.

Best JD Berghmans S Hunt JJFG , et al. (2008) Non-associative learning in larval zebrafish. Neuropsychopharmacology 33: 1206–1215.

Bezerra da Silva C Pott A Elifio-Esposito S , et al. (2016) Effect of donepezil, tacrine, galantamine and rivastigmine on acetylcholinesterase inhibition in Dugesia tigrina. Molecules 21: 53.

Bowers MB Jr Goodman E Sim VM (1964) Some behavioral changes in man following anticholinesterase administration. J Nerv Ment Dis 138: 383–389.

Burt T (2000) Donepezil and related cholinesterase inhibitors as mood and behavioral controlling agents. Curr Psychiatry Rep 2: 473–478.

Canzian J Fontana BD Quadros VA , et al. (2017) Conspecific alarm substance differently alters group behavior of zebrafish populations: Putative involvement of cholinergic and purinergic signaling in anxiety- and fear-like responses. Behav Brain Res 320: 255–263.

Chan AWS Agca Y (2008) Transgenic animal models of neurodegenerative diseases. In: Conn PM (ed.) Sourcebook of Models for Biomedical Research. Totowa: Humana Press, pp. 323–331.

Cho H Lee C-J Choi J , et al. (2012) Anxiolytic effects of an acetylcholinesterase inhibitor, physostigmine, in the adult zebrafish. Anim Cells Syst 16: 198–206.

Christensen DD (2012) Higher-dose (23 mg/day) donepezil formulation for the treatment of patients with moderate-to-severe Alzheimer’s disease. Postgrad Med 124: 110–116.

Chu C-W Liang C-S Wan F-J (2018) Adjunctive donepezil for anxiety symptoms with poor response to paroxetine in a patient with probable mild cognitive impairment. Clin Neuropharmacol 41: 236–237.

Clemente D Porteros A Weruaga E , et al. (2004) Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. J Comp Neurol 474: 75–107.

Colović MB Krstić DZ Lazarević-Pašti TD , et al. (2013) Acetylcholinesterase inhibitors: Pharmacology and toxicology. Curr Neuropharmacol 11: 315–335.

Cummings JL Donohue JA Brooks RL (2000) The relationship between donepezil and behavioral disturbances in patients with Alzheimer’s disease. Am J Geriatr Psychiatry 8: 134–140.

Cutuli D De Bartolo P Caporali P , et al. (2013) Neuroprotective effects of donepezil against cholinergic depletion. Alzheimers Res Ther 5: 50.

Cutuli D Foti F Mandolesi L , et al. (2008) Cognitive performance of healthy young rats following chronic donepezil administration. Psychopharmacology 197: 661–673.

Dawson TM Golde TE Lagier-Tourenne C (2018) Animal models of neurodegenerative diseases. Nat Neurosci 21: 1370–1379.

DeFeudis FV (1974) Chapter 5 - Cholinergic Roles in Motivated Behaviours, Emotion, Learning and Memory. In: DeFeudis FV (ed.) Central Cholinergic Systems and Behaviour. London: Academic Press, pp. 75–121.

DeFeudis FV (2012) Central Cholinergic Systems and Behaviour. Amsterdam: Elsevier.

Demin KA Taranov AS Ilyin NP , et al. (2020) Understanding neurobehavioral effects of acute and chronic stress in zebrafish. Stress. Epub ahead of print 16 March 2020. DOI: 10.1080/10253890.2020.1724948.

Dumitru G El-Nashar HAS Mostafa NM , et al. (2019) Agathisflavone isolated from Schinus polygamus (Cav.) Cabrera leaves prevents scopolamine-induced memory impairment and brain oxidative stress in zebrafish (Danio rerio). Phytomedicine 58: 152889.

Egan RJ Bergner CL Hart PC , et al. (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205: 38–44.

Eissa N Jayaprakash P Azimullah S , et al. (2018) The histamine H3R antagonist DL77 attenuates autistic behaviors in a prenatal valproic acid-induced mouse model of autism. Sci Rep 8: 1–15.

Ellman GL Courtney KD Andres V , et al. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88–95.

English BA Webster AA (2012) Chapter 132 - Acetylcholinesterase and its inhibitors. In: Robertson D Biaggioni I Burnstock G , et al. (eds) Primer on the Autonomic Nervous System. 3rd ed. San Diego: Academic Press, pp. 631–633.

Freeman E Touzel R Grossman A , et al. (1990) Pyridostigmine, an acetylcholinesterase inhibitor, stimulates growth hormone release, but has no effect on basal thyrotrophin or adrenocorticotrophin levels, or the thyrotrophin response to thyrotrophin-releasing hormone. J Neuroendocrinol 2: 429–432.

Furiya Y Tomiyama T Izumi T , et al. (2018) Rivastigmine improves appetite by increasing the plasma acyl/Des-Acyl ghrelin ratio and cortisol in Alzheimer disease. Dement Geriatr Cogn Disord 8: 77–84.

Gauthier S Feldman H Hecker J , et al. (2002) Efficacy of donepezil on behavioral symptoms in patients with moderate to severe Alzheimer’s disease. Int Psychogeriatr 14: 389–404.

Genario R Giacomini AC Demin KA , et al. (2019) The evolutionarily conserved role of melatonin in CNS disorders and behavioral regulation: Translational lessons from zebrafish. Neurosci Biobehav Rev 99: 117–127.

Gerlai R (2014) Social behavior of zebrafish: From synthetic images to biological mechanisms of shoaling. J Neurosci Methods 234: 59–65.

Giacomini A Abreu MS Giacomini LV , et al. (2016) Fluoxetine and diazepam acutely modulate stress induced-behavior. Behav Brain Res 296: 301–310.

Giménez-Llort L Ratia M Pérez B , et al. (2017) Behavioural effects of novel multitarget anticholinesterasic derivatives in Alzheimer’s disease. Behav Pharmacol 28: 124–131.

Gouveia MK Miguel TT Busnardo C , et al. (2016) Dissociation in control of physiological and behavioral responses to emotional stress by cholinergic neurotransmission in the bed nucleus of the stria terminalis in rats. Neuropharmacology 101: 379–388.

Hara Y Kawabe H (2019) Donepezil (Aricept). In: Nagaoka S (ed.) Drug Discovery in Japan: Investigating the Sources of Innovation. Singapore: Springer Singapore, pp. 183–205.

Hasey G Hanin I (1990) Plasma corticosterone is increased and correlated with brain acetylcholine in physostigmine- but not in neostigmine-treated rats. Psychoneuroendocrinology 15: 357–369.

Haverroth GMB Welang C Mocelin RN , et al. (2015) Copper acutely impairs behavioral function and muscle acetylcholinesterase activity in zebrafish (Danio rerio). Ecotoxicol Environ Saf 122: 440–447.

Hernandez CM Gearhart DA Parikh V , et al. (2006) Comparison of galantamine and donepezil for effects on nerve growth factor, cholinergic markers, and memory performance in aged rats. J Pharmacol Exp Ther 316: 679–694.

Howard RJ Juszczak E Ballard CG , et al. (2007) Donepezil for the treatment of agitation in Alzheimer’s disease. N Engl J Med 357: 1382–1392.

Howe K Clark MD Torroja CF , et al. (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496: 498–503.

Ishikawa K Motoi Y Mizuno Y , et al. (2014) Effects of donepezil dose escalation in Parkinson’s patients with dementia receiving long-term donepezil treatment: An exploratory study. Psychogeriatrics 14: 93–100.

Janowsky DS Risch SC (1984) Cholinomimetic and anticholinergic drugs used to investigate an acetylcholine hypothesis of affective disorders and stress. Drug Dev Res 4: 125–142.

Jelic V Darreh-Shori T (2010) Donepezil: A review of pharmacological characteristics and role in the management of Alzheimer disease. Clin Med Insights Ther 2: 771–788.

Kacprzak V Patel NA Riley E , et al. (2017) Dopaminergic control of anxiety in young and aged zebrafish. Pharmacol Biochem Behav 157: 1–8.

Kalueff AV Gebhardt M Stewart AM , et al. (2013) Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 10: 70–86.

Kant GJ Bauman RA Feaster SR , et al. (2001) The combined effects of pyridostigmine and chronic stress on brain cortical and blood acetylcholinesterase, corticosterone, prolactin and alternation performance in rats. Pharmacol Biochem Behav 70: 209–218.

Kasa P Papp H Kasa P , et al. (2000) Donepezil dose-dependently inhibits acetylcholinesterase activity in various areas and in the presynaptic cholinergic and the postsynaptic cholinoceptive enzyme-positive structures in the human and rat brain. Neuroscience 101: 89–100.

Kennedy B Janowsky DS Risch SC , et al. (1984) Central cholinergic stimulation causes adrenal epinephrine release. J Clin Investig 74: 972–975.

Khachaturian ZS Radebaugh TS (2019) Alzheimer’s Disease: Cause (s), Diagnosis, Treatment, and Care. Boca Raton: CRC Press.

Khan KM Collier AD Meshalkina DA , et al. (2017) Zebrafish models in neuropsychopharmacology and CNS drug discovery. Br J Pharmacol 174: 1925–1944.

Kim Y-H Lee Y Kim D , et al. (2010) Scopolamine-induced learning impairment reversed by physostigmine in zebrafish. Neurosci Res 67: 156–161.

Kysil EV Meshalkina DA Frick EE , et al. (2017) Comparative analyses of zebrafish anxiety-like behavior using conflict-based novelty tests. Zebrafish 14: 197–208.

Kyzar EJ Collins C Gaikwad S , et al. (2012) Effects of hallucinogenic agents mescaline and phencyclidine on zebrafish behavior and physiology. Prog Neuropsychopharmacol Biol Psychiatry 37: 194–202.

Lee JH Jeong SK Kim BC , et al. (2015) Donepezil across the spectrum of Alzheimer’s disease: Dose optimization and clinical relevance. Acta Neurol Scand 131: 259–267.

Liang YQ Tang XC (2006) Comparative studies of huperzine A, donepezil, and rivastigmine on brain acetylcholine, dopamine, norepinephrine, and 5-hydroxytryptamine levels in freely-moving rats. Acta Pharmacologica Sinica 27: 1127–1136.

Luzeena Raja G Divya Subhashree K Lite C , et al. (2019) Transient exposure of methylparaben to zebrafish (Danio rerio) embryos altered cortisol level, acetylcholinesterase activity and induced anxiety-like behaviour. Gen Comp Endocrinol 279: 53–59.

Mans RA Hinton KD Payne CH , et al. (2019) Cholinergic stimulation of the adult zebrafish brain induces phosphorylation of glycogen synthase kinase-3 β and extracellular signal-regulated kinase in the telencephalon. Front Mol Neurosci 12: 91.

Mega MS Masterman DM O’Connor SM , et al. (1999) The spectrum of behavioral responses to cholinesterase inhibitor therapy in Alzheimer disease. Arch Neurol 56: 1388–1393.

Miller N Gerlai R (2007) Quantification of shoaling behaviour in zebrafish (Danio rerio). Behav Brain Res 184: 157–166.

Miller N Gerlai R (2012) From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio). PLoS One 7: e48865.

Mineur YS Obayemi A Wigestrand MB , et al. (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci 110: 3573.

Mueller T Vernier P Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011: 156–169.

Muthuraman A Nafisa K Sowmya MS , et al. (2019) Role of ambrisentan (selective endothelin-A receptor antagonist) on cigarette smoke exposure induced cognitive impairment in Danio rerio. Life Sci 222: 133–139.

Nicolodi M Galeotti N Ghelardini C , et al. (2002) Central cholinergic challenging of migraine by testing second-generation anticholinesterase drugs. Headache 42: 596–602.

Parker MO Brock AJ Sudwarts A , et al. (2015) Developmental role of acetylcholinesterase in impulse control in zebrafish. Front Behav Neurosci 9: 271.

Parng C Seng WL Semino C , et al. (2002) Zebrafish: A preclinical model for drug screening. Assay Drug Dev Technol 1: 41–48.

Pompeia S Gouveia JR Galduróz JCF (2013) Acute mood effect of donepezil in young, healthy volunteers. Hum Psychopharmacol Clin Exp 28: 263–269.

Poole RL Connor DA Gould TJ (2014) Donepezil reverses nicotine withdrawal-induced deficits in contextual fear conditioning in C57BL/6J mice. Behav Neurosci 128: 588–593.

Raghavendra M Maiti R Kumar S , et al. (2013) Role of aqueous extract of Azadirachta indica leaves in an experimental model of Alzheimer’s disease in rats. Int J Appl Basic Med Res 3: 37–47.

Rawashdeh O de Borsetti NH Roman G , et al. (2007) Melatonin suppresses nighttime memory formation in zebrafish. Science 318: 1144–1146.

Riedel G Kang SH Choi DY , et al. (2009) Scopolamine-induced deficits in social memory in mice: Reversal by donepezil. Behav Brain Res 204: 217–225.

Risch SC Cohen RM Janowsky DS , et al. (1980) Mood and behavioral effects of physostigmine on humans are accompanied by elevations in plasma beta-endorphin and cortisol. Science 209: 1545–1546.

Rosa LV Costa FV Canzian J , et al. (2020) Three- and bi-dimensional analyses of the shoaling behavior in zebrafish: Influence of modulators of anxiety-like responses. Prog Neuropsychopharmacol Biol Psychiatry 102: 109957.

San Chang Y Wu YH Wang CJ , et al. (2018) Higher levels of thyroxine may predict a favorable response to donepezil treatment in patients with Alzheimer disease: A prospective, case–control study. BMC Neurosci 19: 36.

Schrag A (2004) Psychiatric aspects of Parkinson’s disease–an update. J Neurol 251: 795–804.

Seltzer B (2007) Donepezil: An update. Expert Opin Pharmacother 8: 1011–1023.

Shin CY Kim H-S Cha K-H , et al. (2018) The effects of donepezil, an acetylcholinesterase inhibitor, on impaired learning and memory in rodents. Biomol Ther 26: 274–281.

Silman I Sussman JL (2008) Acetylcholinesterase: How is structure related to function? Chem Biol Interact 175: 3–10.

Sink TD Lochmann RT Fecteau KA (2008) Validation, use, and disadvantages of enzyme-linked immunosorbent assay kits for detection of cortisol in channel catfish, largemouth bass, red pacu, and golden shiners. Fish Physiol Biochem 34: 95–101.

Soliani A Kubota SM Corrêa MF , et al. (2020) Differential contribution of H(3)R antagonism by LINS01 compounds on memory, anxiety-like behaviour and spontaneous locomotor activity in healthy rats. Behav Brain Res 377: 112230.

Song C Liu B-P Zhang Y-P , et al. (2018) Modeling consequences of prolonged strong unpredictable stress in zebrafish: Complex effects on behavior and physiology. Prog Neuropsychopharmacol Biol Psychiatry 81(Suppl C): 384–394.

Song C Yang L Wang J , et al. (2016) Building neurophenomics in zebrafish: Effects of prior testing stress and test batteries. Behav Brain Res 311: 24–30.

Stewart A Gaikwad S Kyzar E , et al. (2012) Modeling anxiety using adult zebrafish: A conceptual review. Neuropharmacology 62: 135–143.

Stewart AM Gerlai R Kalueff AV (2015) Developing highER-throughput zebrafish screens for in-vivo CNS drug discovery. Front Behav Neurosci 9: 14.

Suarez-Lopez JR Hood N Suárez-Torres J , et al. (2019) Associations of acetylcholinesterase activity with depression and anxiety symptoms among adolescents growing up near pesticide spray sites. Int J Hyg Environ Health 222: 981–990.

Weiner MF Martin-Cook K Foster BM , et al. (2000) Effects of donepezil on emotional/behavioral symptoms in Alzheimer’s disease patients. J Clin Psychiat 61: 487–492.

Ye CY Lei Y Tang XC , et al. (2015) Donepezil attenuates Aβ-associated mitochondrial dysfunction and reduces mitochondrial Aβ accumulation in vivo and in vitro. Neuropharmacology 95: 29–36.

Zhang T Peterson RT (2020) Chapter 51 - Zebrafish as a platform for drug screening. In: Cartner SC Eisen JS Farmer SC , et al. (eds) The Zebrafish in Biomedical Research. Cambridge, MA: Academic Press, pp. 659–675.

Zhang L Zhou FM Dani JA (2004) Cholinergic drugs for Alzheimer’s disease enhance in vitro dopamine release. Mol Pharmacol 66: 538–544.