Selective activation of D1 dopamine receptors exerts antidepressant-like activity in rats

Abstract

Background:

Major depressive disorder is a common illness that severely decreases psychosocial functioning. Due to the major limitations of current treatments including response failure, it is crucial to develop better therapy strategies. Evidence suggests that dopamine dysregulation might play a major role in major depressive disorder physiopathology.

Aims:

This study investigates whether the dopamine D1 receptor agonist A77636 modulates antidepressant-like activity in rats.

Methods:

Rats were injected with an acute single dose of A77636 (0.75, 1.5 or 3 mg/kg), a potent and selective dopamine D1-like receptor agonist. Their locomotor activity, social interactions and behavioural response to the forced swim test were analysed 30 min after the injection.

Results:

During the forced swim test, the D1 agonist dose dependently reduced the immobility while the time of bursting was increased. Social interactions were significantly increased in the animals exposed to 3 mg/kg of A77636 whereas no significant changes were measured in general motor activity.

Conclusions:

The present results provide evidence that pharmacological modulation of D1 receptor by the selective agonist A77636 induces antidepressant-like effects in rats, which encourages further studies regarding D1-specific modulation in major depressive disorder treatment.

Keywords

Dopamine D1-agonist antidepressant forced swim test (FST)social interactions

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References

Admon

Kaiser

Dillon

, et al. (2017) Dopaminergic enhancement of striatal response to reward in major depression. Am J Psychiatry 174: 378–386.

Anyan

Amir

(2018) Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology 43: 931–933.

Argyropoulos

Nutt

(2013) Anhedonia revisited: Is there a role for dopamine-targeting drugs for depression? J Psychopharmacol 27: 869–877.

Belujon

Grace

(2017) Dopamine system dysregulation in major depressive disorders. Int J Neuropsychopharmacol 20: 1036–1046.

Berton

Nestler

(2006) New approaches to antidepressant drug discovery: Beyond monoamines. Nat Rev Neurosci 7(2): 137–151.

Bourin

Colombel

Redrobe

, et al. (1998) Evaluation of efficacies of different classes of antidepressants in the forced swimming test in mice at different ages. Prog Neuro-Psychoph 22: 343–351.

Bruns

Mitchell

Wafford

, et al. (2018) Preclinical profile of a dopamine D1 potentiator suggests therapeutic utility in neurological and psychiatric disorders. Neuropharmacology 128: 351–365.

Cadeddu

Ibba

Sadile

, et al. (2014) Antidepressants share the ability to increase catecholamine output in the bed nucleus of stria terminalis: A possible role in antidepressant therapy? Psychopharmacology 231: 1925–1933.

Carr

Kim

G-Y

de Vaca

(2001) Rewarding and locomotor-activating effects of direct dopamine receptor agonists are augmented by chronic food restriction in rats. Psychopharmacology 154: 420–428.

10.

Chaudhury

Walsh

Friedman

, et al. (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493: 532–536.

11.

Chausmer

Katz

(2002) Comparison of interactions of D 1-like agonists, SKF 81297, SKF 82958 and A-77636, with cocaine: Locomotor activity and drug discrimination studies in rodents. Psychopharmacology 159: 145–153.

12.

Cipriani

Furukawa

Salanti

, et al. (2018) Comparative efficacy and acceptability of 21 antidepressant drugs for the acute treatment of adults with major depressive disorder: A systematic review and network meta-analysis. Lancet 391: 1357–1366.

13.

Czéh

Fuchs

Wiborg

, et al. (2016) Animal models of major depression and their clinical implications. Prog Neuropsychopharmacol Biol Psychiatry 64: 293–310.

14.

D’Aquila

Collu

Pani

, et al. (1994) Antidepressant-like effect of selective dopamine D1 receptor agonists in the behavioural despair animal model of depression. Eur J Pharmacol 262: 107–111.

15.

de Kloet

Molendijk

(2016) Coping with the forced swim stressor: Towards understanding an adaptive mechanism. Neural Plast 2016: 6503162.

16.

DeNinno

Schoenleber

MacKenzie

, et al. (1991) A68930: A potent agonist selective for the dopamine D1 receptor. Eur J Pharmacol 199: 209–219.

17.

Di Chiara

(1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375: 13–30.

18.

Dunlop

Nemeroff

(2007) The role of dopamine in the pathophysiology of depression. Arch Gen Psychiatry 64: 327–337.

19.

Esumi

Kawasaki

Nakamoto

, et al. (2013) Differential effects of nomifensine and imipramine on motivated behavior in the runway model of intracranial self-stimulation. Eur J Pharmacol 720: 186–191.

20.

Friedman

Walsh

Juarez

, et al. (2014) Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science 344: 313–319.

21.

Gambarana

Ghiglieri

Tagliamonte

, et al. (1995) Crucial role of D1 dopamine receptors in mediating the antidepressant effect of imipramine. Pharmacol Biochem Behav 50: 147–151.

22.

Golden

Covington

Berton

, et al. (2011) A standardized protocol for repeated social defeat stress in mice. Nat Protoc 6: 1183–1191.

23.

Gunaydin

Grosenick

Finkelstein

, et al. (2014) Natural neural projection dynamics underlying social behavior. Cell 157: 1535–1551.

24.

Hao

Beck

Schaus

, et al. (2019) Synthesis and pharmacological characterization of 2-(2,6-dichlorophenyl)-1-((1S,3R)-5-(3-hydroxy-3-methylbutyl)-3-(hydroxymethyl)-1-methyl-3,4-dihydroisoquinolin-2(1H)-yl)ethan-1-one (LY3154207), a potent, subtype selective, and orally available positive allosteric modulator of the human dopamine D1 receptor. J Med Chem 62: 8711–8732.

25.

Hare

Shinohara

Liu

, et al. (2019) Optogenetic stimulation of medial prefrontal cortex Drd1 neurons produces rapid and long-lasting antidepressant effects. Nat Commun 10: 1–12.

26.

Hori

Kunugi

(2013) Dopamine agonist-responsive depression. Psychogeriatrics 13: 189–195.

27.

Ichikawa

Meltzer

(1995) Effect of antidepressants on striatal and accumbens extracellular dopamine levels. Eur J Pharmacol 281: 255–261.

28.

Isacson

Kull

Wahlestedt

, et al. (2004) A 68930 and dihydrexidine inhibit locomotor activity and d-amphetamine-induced hyperactivity in rats: A role of inhibitory dopamine d1/5 receptors in the prefrontal cortex? Neuroscience 124: 33–42.

29.

Jay

Rocher

Hotte

, et al. (2004) Plasticity at hippocampal to prefrontal cortex synapses is impaired by loss of dopamine and stress: Importance for psychiatric diseases. Neurotox Res 6: 233–244.

30.

Kessler

Bromet

(2013) The epidemiology of depression across cultures. Annu Rev Public Health 34: 119–138.

31.

Kokkinou

Ashok

Howes

(2018) The effects of ketamine on dopaminergic function: Meta-analysis and review of the implications for neuropsychiatric disorders. Mol Psychiatry 23: 59–69.

32.

Lavergne

Jay

(2010) A new strategy for antidepressant prescription. Front Neurosci 4: 192.

33.

Malhi

Mann

(2018) Depression. Lancet 392: 2299–2312.

34.

Matta

Tiessen

Choleris

(2017) The role of dorsal hippocampal dopamine D1-type receptors in social learning, social interactions, and food intake in male and female mice. Neuropsychopharmacology 42: 2344–2353.

35.

Mattingly

Rowlett

Lovell

(1993) Effects of daily SKF 38393, quinpirole, and SCH 23390 treatments on locomotor activity and subsequent sensitivity to apomorphine. Psychopharmacology 110: 320–326.

36.

Molendijk

de Kloet

(2019) Coping with the forced swim stressor: Current state-of-the-art. Behav Brain Res 364: 1–10.

37.

Pizzagalli

Berretta

Wooten

, et al. (2019) Assessment of striatal dopamine transporter binding in individuals with major depressive disorder: In vivo positron emission tomography and postmortem evidence. JAMA Psychiatry 76: 854–861.

38.

Plavén-Sigray

Gustavsson

Farde

, et al. (2014) Dopamine D1 receptor availability is related to social behavior: A positron emission tomography study. NeuroImage 102: 590–595.

39.

Porsolt

Le Pichon

Jalfre

(1977) Depression: A new animal model sensitive to antidepressant treatments. Nature 266: 730–732.

40.

Randrup

(1975) Mania, depression, and brain dopamine. In: Essman WB and Valzelli S (eds) Current Development in Psychopharmacology. New York: Spectrum Publications, pp. 206–248.

41.

Roberts

Seymour

Schmidt

, et al. (2010) Amelioration of ketamine-induced working memory deficits by dopamine D1 receptor agonists. Psychopharmacology 210: 407–418.

42.

Rocher

Spedding

Munoz

, et al. (2004) Acute stress-induced changes in hippocampal/prefrontal circuits in rats: Effects of antidepressants. Cereb Cortex 14: 224–229.

43.

Rush

Trivedi

Wisniewski

, et al. (2006) Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: A STAR*D report. Am J Psychiatry 163: 1905–1917.

44.

Sampson

Willner

Muscat

(1991) Reversal of antidepressant action by dopamine antagonists in an animal model of depression. Psychopharmacology 104: 491–495.

45.

Scheggi

De Montis

Gambarana

(2018) Making sense of rodent models of anhedonia. Int J Neuropsychopharmacol 21: 1049–1065.

46.

Schneier

Slifstein

Whitton

, et al. (2018) Dopamine release in antidepressant-naive major depressive disorder: A multimodal [11C]-(+)-PHNO positron emission tomography and functional magnetic resonance imaging study. Biol Psychiatry 84: 563–573.

47.

Shuto

Kuroiwa

Sotogaku

, et al. (2018) Obligatory roles of dopamine D1 receptors in the dentate gyrus in antidepressant actions of a selective serotonin reuptake inhibitor, fluoxetine. Mol Psychiatr 25: 1229–1244.

48.

Slattery

Cryan

(2012) Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc 7: 1009–1014.

49.

Stuchlik

Vales

(2006) Effect of dopamine D1 receptor antagonist SCH23390 and D1 agonist A77636 on active allothetic place avoidance, a spatial cognition task. Behav Brain Res 172: 250–255.

50.

Svensson

Hao

Bruns

(2019) Positive allosteric modulators of the dopamine D1 receptor: A new mechanism for the treatment of neuropsychiatric disorders. Adv Pharmacol 86: 273–305.

51.

Tye

Mirzabekov

Warden

, et al. (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493: 537–541.

52.

Willner

(2016) The chronic mild stress (CMS) model of depression: History, evaluation and usage. Neur Stress 6: 78–93.

53.

Yadid

Friedman

(2008) Dynamics of the dopaminergic system as a key component to the understanding of depression. Prog Brain Res 172: 265–286.

54.

Yamada

Sugimoto

Yamada

(2004) Involvement of dopamine receptors in the anti-immobility effects of dopamine re-uptake inhibitors in the forced swimming test. Eur J Pharmacol 504: 207–211.