Mice Lacking TAAR1 Show No Early Behavioral Response to Acute Restraint Stress
- Autores: Aleksandrov A.1, Vinogradova E.1, Simon Y.1, Aleksandrov A.1, Knyazeva V.1, Stankevich L.1, Kozyreva A.1
-
Afiliações:
- Saint Petersburg State University
- Edição: Volume 109, Nº 11 (2023)
- Páginas: 1650-1664
- Seção: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
- URL: https://journals.rcsi.science/0869-8139/article/view/232281
- DOI: https://doi.org/10.31857/S0869813923110122
- EDN: https://elibrary.ru/YBSPJG
- ID: 232281
Citar
Resumo
The role of the TAAR1 receptor, one of the trace amine-associated receptors (TAARs) family, in the formation of the behavioral component of the stress response was studied. The behavior of female TAAR1 knockout mice and wild-type (WT) mice was investigated in tests of elevated plus maze and elevated zero maze (EPM and EZM) and forced swimming test (FST) under normal conditions and after uncontrolled restraint stress exposure for 30 min. In the EPM test, the initial level of locomotor and exploratory activity, as well as the anxiety, was identical in both groups of mice. In the EZM test, the initial indicators of anxiety in female TAAR1 KO mice compared to female WT mice were higher, and locomotor activity was lower. When testing mice in the EZM 30 minutes after the end of stress exposure, it was found that the anxiety in female WT mice sharply increased, and the indicators of locomotor activity and exploratory behavior significantly decreased. The behavioral indicators in the EZM test in TAAR1 KO mice before and after stress were identical. A pronounced behavioral component of the stress response was observed in both TAAR1 KO and WT mice during testing in EPM. There were no significant differences between TAAR1 KO and WT mice during testing in EPM four hours after stress exposure. In the FST test the latency to the first immobility was initially longer in TAAR1 KO mice compared to the WT mice, but 24 h after the stress this indicator has significantly decreased. As a result, TAAR1 KO and WT mice no longer differed in all behavioral indicators in the FST. Three weeks after acute restraint stress, both TAAR1 KO and WT groups showed a significant increase in immobility duration and a decrease in latency to the first immobility, however no difference between the both groups of animals were found. Thereby, we found the complete absence of behavioral change immediately after stressor exposure in TAAR1 KO compared to the WT mice.
Sobre autores
A. Aleksandrov
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
E. Vinogradova
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
Yu. Simon
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
A. Aleksandrov
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
V. Knyazeva
Saint Petersburg State University
Autor responsável pela correspondência
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
L. Stankevich
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
A. Kozyreva
Saint Petersburg State University
Email: v.m.knyazeva@spbu.ru
Russia, St Petersburg
Bibliografia
- Lindemann L, Hoener MC (2005) A renaissance in trace amines inspired by a novel GPCR family. Trends Pharmacol Sci 26: 274–281. https://doi.org/10.1016/j.tips.2005.03.007
- Berry MD, Gainetdinov RR, Hoener MC, Shahid M (2017) Pharmacology of human trace amine-associated receptors: therapeutic opportunities and challenges. Pharmacol Ther 180: 161–180. https://doi.org/10.1016/j.pharmthera.2017.07.002
- Rutigliano G, Accorroni A, Zucchi R (2018) The case for TAAR1 as a modulator of central nervous system function. Front Pharmacol 8: 987. https://doi.org/10.3389/fphar.2017.00987
- Gainetdinov RR, Hoener MC, Berry MD (2003) Trace Amines and Their Receptors. Pharmacol Rev (2018) 70(3): 549–620. https://doi.org/10.1124/pr.117.015305
- Branchek TA, Blackburn TP Trace amine receptors as targets for novel therapeutics: legend, myth and fact. Curr Opin Pharmacol 3(1): 90–97. https://doi.org/10.1016/s1471-4892(02)00028-0
- Pei Y, Asif-Malik A, Canales JJ (2016) Trace amines and the trace amine-associated receptor 1: pharmacology, neurochemistry, and clinical implications. Front Neurosci 10: 148. https://doi.org/10.3389/fnins.2016.00148
- Berry MD (2007) The potential of trace amines and their receptors for treating neurological and psychiatric diseases. Rev Recent Clin Trials 2(1): 3–19. https://doi.org/10.2174/157488707779318107
- Sotnikova TD, Caron MG, Gainetdinov RR (2009) Trace Amine-Associated Receptors as Emerging Therapeutic Targets. Mol Pharmacol 76(2): 229–235. https://doi.org/10.1124/mol.109.055970
- Rutigliano G, Zucchi R (2020) Molecular Variants in Human Trace Amine-Associated Receptors and Their Implications in Mental and Metabolic Disorders. Cell Mol Neurobiol 40(2): 239–255. https://doi.org/10.1007/s10571-019-00743-y
- Revel FG, Moreau JL, Gainetdinov RR, Bradaia A, Sotnikova TD, Mory R, Durkin S, Zbinden KG, Norcross R, Meyer CA, Metzler V, Chaboz S, Ozmen L, TrubeG, Pouzet B, Bettler B, Caron MG, Wettstein JG, Hoener MC (2011) TAAR1 activation modulates monoaminergic neurotransmission, preventing hyperdopaminergic and hypoglutamatergic activity. Proc Natl Acad Sci U S A 108(20): 8485–8490. https://doi.org/10.1073/pnas.1103029108
- Revel FG, Moreau JL, Gainetdinov RR, Ferragud A, Velázquez-Sánchez C, Sotnikova TD, Morairty SR, Harmeier A, Zbinden GK, Norcross RD, Bradaia A, Kilduff TS, Biemans B, Pouzet B, Caron MG, Canales JJ, Wallace TL, Wettstein JG, Hoener MC (2012) Trace amine-associated receptor 1 partial agonism reveals novel paradigm for neuropsychiatric therapeutics. Biol Psychiatry 72: 934–942. https://doi.org/10.1016/j.biopsych.2012.05.014
- Revel FG, Moreau JL, Pouzet B, Mory R, Bradaia A, Buchy D, Metzler V, Chaboz S, Groebke Zbinden K, Galley G, Norcross RD, Tuerck D, Bruns A, Morairty SR, Kilduff TS, Wallace TL, Risterucci C, Wettstein JG, Hoener MC (2013) A new perspective for schizophrenia: TAAR1 agonists reveals antipsychotic- and antidepressant-like activity, improve cognition and control body weight. Mol Psychiatry 18: 543–556. https://doi.org/10.1038/mp.2012.57
- Lopez AD, Murray CC (1998) The global burden of disease, 1990–2020. Nat Med 4: 1241–1243. https://doi.org/10.1038/3218
- Kessler RC, Berglund P, Demler O, Jin R, Koretz D, Merikangas KR, Rush AJ, Walters EE, Wang PS (2003) The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). Jama 289: 3095–3105. https://doi.org/10.1001/jama.289.23.3095
- Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455: 894–902. https://doi.org/10.1038/nature07455
- Pizzagalli DA (2014) Depression, stress, and anhedonia: toward a synthesis and integrated model. Ann Rev Clin Psychol 10: 393–423. https://doi.org/10.1146/annurev-clinpsy-050212-185606
- Hao Y, Ge H, Sun M, Gao Y (2019) Selecting an Appropriate Animal Model of Depression. Int J Mol Sci 20: 4827. https://doi.org/10.3390/ijms20194827
- Cryan JF, Mombereau C (2004) In search of a depressed mouse: utility of models for studying depression-related behavior in genetically modified mice. Mol Psychiatry 9: 326–357. https://doi.org/10.1038/sj.mp.4001457
- Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455: 89–902. https://doi.org/10.1038/nature07455
- Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB (1993) Sex and depression in the National Comorbidity Survey I: Lifetime prevalence, chronicity and recurrence. J Affect Disord 29: 85–96. https://doi.org/10.1016/0165-0327(93)90026-g
- McEwen BS, Milner TA (2017) Understanding the Broad Influence of Sex Hormones and Sex Differences in the Brain. J Neurosci Res 95: 24–39. https://doi.org/10.1002/jnr.23809
- European Convention for the Protection of Vertebrate Animals Used for Experimentation and other Scientific Purposes. 1986.
- Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2: 322–328. https://doi.org/10.1038/nprot.2007.44
- Pellow S, File SE (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24(3): 525–529. https://doi.org/10.1016/0091-3057(86)90552-6
- Braun AA, Skelton MR, Vorhees CV, Williams MT (2011) Comparison of the elevated plus and elevated zero mazes in treated and untreated male Sprague-Dawley rats: Effects of anxiolytic and anxiogenic agents. Pharmacol Biochem Behav 97(3): 406–415. https://doi.org/10.1016/j.pbb.2010.09.013
- Can A, Dao DT, Arad M, Terrillion CE, Piantadosi SC, Gould TD (2012) The Mouse Forced Swim Test. J Vis Exp 59: e3638. https://doi.org/10.3791/3638
- Yankelevitch-Yahav R, Franko M, Huly A, Doron R (2015) The Forced Swim Test as a Model of Depressive-like Behavior. J Vis Exp 97: e52587. https://doi.org/10.3791/52587
- Birmann PT, Domingues M, Casaril AM, Smaniotto TA, Hartwig D, Jacob RG, Savegnago L (2021) A pyrazole-containing selenium compound modulates neuroendocrine, oxidative stress, and behavioral responses to acute restraint stress in mice. Behav Brain Res 396: 112874. https://doi.org/10.1016/j.bbr.2020.112874
- Galeeva A, Tuohimaa P (2001) Analysis of mouse plus-maze behavior modulated by ovarian steroid. Behav Brain Res 119(1): 41–47. https://doi.org/10.1016/s0166-4328(00)00341-7
- Виноградова ЕП, Зайченко ИН, Жуков ДА (1996) Влияние стресса на уровень тревожности у самок белых крыс в различные стадии эстрального цикла. Журн высш нервн деятельн им ИП Павлова 46(4): 769–775. [Vinogradova EP, Zaichenko IN, Zhukov DA (1996) The effect of stress on the anxiety level in female white rats at different stages of the estrous cycle. Zh Vyssh Nerv Deiat im IP Pavlova 46(4): 769–775. (In Russ)].
- Scholl JL, Afzal A, Fox LC, Watt MJ, Forster GL (2019) Sex differences in anxiety-like behaviors in rats. Physiol Behav 211: 112670. https://doi.org/10.1016/j.physbeh.2019.112670
- Cora MC, Kooistra L, Travlos G (2015) Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol Pathol 43: 776–793. https://doi.org/10.1177/0192623315570339
- Felicio LS, Nelson JF, Finch CE (1984) Longitudinal studies of estrous cyclicity in aging C57BL/6J mice: II. Cessation of cyclicity and the duration of persistent vaginal cornification. Biol Reprod 31: 446–453. https://doi.org/10.1095/biolreprod31.3.446
- Wolinsky TD, Swanson CJ, Smith KE, Zhong H, Borowsky B, Seeman P, Branchek T, Gerald CP (2007) The Trace Amine 1 receptor knockout mouse: an animal model with relevance to schizophrenia. Genes Brain Behav 6(7): 628–639. https://doi.org/10.1111/j.1601-183X.2006.00292.x
- Zhukov IS, Karpova IV, Krotova NA, Tissen IY, Demin KA, Shabanov PD, Budygin EA, Kalueff AV, Gainetdinov RR (2022) Enhanced Aggression, Reduced Self-Grooming Behavior and Altered 5‑HT Regulation in the Frontal Cortex in Mice Lacking Trace Amine-Associated Receptor 1 (TAAR1). Int J Mol Sci 23(22): 14066. https://doi.org/10.3390/ijms232214066
- Kulkarni SK, Singh K, Bishnoi M (2007) Elevated zero maze: a paradigm to evaluate antianxiety effects of drugs. Methods Find Exp Clin Pharmacol 29: 343–348. https://doi.org/10.1358/mf.2007.29.5.1117557
- Tucker LB, McCabe JT (2017) Behavior of Male and Female C57BL/6J Mice Is More Consistent with Repeated Trials in the Elevated Zero Maze than in the Elevated Plus Maze. Front Behav Neurosci 11: 13. https://doi.org/10.3389/fnbeh.2017.00013
- Liu J, Hester K, Pope C (2021) Dose- and time-related effects of acute diisopropylfluorophosphate intoxication on forced swim behavior and sucrose preference in rats. Neurotoxicology 82: 82–88. https://doi.org/10.1016/j.neuro.2020.11.007
- Armario A, Gavalda A, Marti J (1995) Comparison of the behavioural and endocrine to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 20: 879–890. https://doi.org/10.1016/0306-4530(95)00018-6
- Swiergiel AH, Leskov IL, Dunn AJ (2008) Effects of chronic and acute stressors and CRF on depression-like behavior in mice. Behav Brain Res 186(1): 32–40. https://doi.org/10.1016/j.bbr.2007.07.018
- Tang J, Yu W, Chen S, Gao Z, Xiao B (2018) Microglia Polarization and Endoplasmic Reticulum Stress in Chronic Social Defeat Stress Induced Depression, Mouse. Neurochem Res 43: 985–994. https://doi.org/10.1007/s11064-018-2504-0
- Leschik J, Gentile A, Cicek C, P’eron S, Tevosian M, Beer A, Radyushkin K, Bludau A, Ebner K, Neumann I, Singewald N, Berninger B, Lessmann V, Lutz B (2022) Brain-derived neurotrophic factor expression in serotonergic neurons improves stress resilience and promotes adult hippocampal neurogenesis. Progr Neurobiol 217: 102333. https://doi.org/10.1016/j.pneurobio.2022.102333
- Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U (2005) Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 162: 127–134. https://doi.org/10.1016/j.bbr.2005.03.009
- Overstreet DH, Friedman E, Mathé AA, Yadid G (2005) The Flinders Sensitive Line rat: a selectively bred putative animal model of depression. Neurosci Biobehav Rev 29: 739–759. https://doi.org/10.1016/j.neubiorev.2005.03.015
- Commons KG, Cholanians AB, Babb JA, Ehlinger DG (2017) The Rodent Forced Swim Test Measures Stress-Coping Strategy, Not Depression-like Behavior. ACS Chem Neurosci 8: 955–960. https://doi.org/10.1021/acschemneuro.7b00042
- de Kloet ER, Molendijk ML (2016) Coping with the Forced Swim Stressor: Towards Understanding an Adaptive Mechanism. Neural Plasticity 2016: 6503162. https://doi.org/10.1155/2016/6503162
- Koob GF (1999) Corticotropin-releasing factor, norepinephrine, and stress. Biol Psychiatry 46: 1167–1180. https://doi.org/10.1016/s0006-3223(99)00164-x
- Stanton LM, Price AJ, Manning EE (2023) Hypothalamic corticotrophin releasing hormone neurons in stress-induced psychopathology: Revaluation of synaptic contributions. J Neuroendocrinol 35: e13268. https://doi.org/10.1111/jne.13268
- Valentino RJ, Rudoy C, Saunders A, Liu XB, Van Bockstaele EJ (2001) Corticotropin-releasing factor is preferentially colocalized with excitatory rather than inhibitory amino acids in axon terminals in the peri-locus coeruleus region. Neuroscience 106: 375–384. https://doi.org/10.1016/s0306-4522(01)00279-2
- Gallagher JP, Orozco-Cabal LF, Liu J, Shinnick-Gallagher P (2008) Synaptic physiology of central CRH system. Eur J Pharmacol 583: 215–225. https://doi.org/10.1016/j.ejphar.2007.11.075
- Mazzitelli M, Yakhnitsa V, Neugebauer B, Neugebauer V (2022) Optogenetic manipulations of CeA-CRF neurons modulate pain- and anxiety-like behaviors in neuropathic pain and control rats. Neuropharmacology 210: 109031. https://doi.org/10.1016/j.neuropharm.2022.109031
- Paretkara T, Dimitrova E (2018) The central amygdala corticotropin-releasing hormone (CRH) neurons modulation of anxiety-like behavior and hippocampus-dependent memory in mice. Neuroscience 390: 187–197. https://doi.org/10.1016/j.neuroscience.2018.08.019
- Holsboer F, Ising M (2008) Central CRH system in depression and anxiety-evidence from clinical studies with CRH1. Eur J Pharmacol 583: 350–357. https://doi.org/10.1016/j.ejphar.2007.12.032
- Henckens MJ, Deussing JM, Chen A (2016) Region-specific roles of the corticotropin-releasing factor-urocortin system in stress. Nat Rev Neurosci 17: 636–651. https://doi.org/10.1038/nrn.2016.94
- Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, Scheimann J, Myers B (2016) Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. Compr Physiol 6: 603–621. https://doi.org/10.1002/cphy.c150015
- Blank T, Nijholt I, Grammatopoulos DK, Randeva HS, Hillhouse E, Spiess J (2003) Corticotropin-Releasing Factor Receptors Couple to Multiple G-Proteins to Activate Diverse Intracellular Signaling Pathways in Mouse Hippocampus: Role in Neuronal Excitability and Associative Learning. J Neurosci 23: 700–707. https://doi.org/10.1523/JNEUROSCI.23-02-00700.2003
- Blank T, Nijholt I, Eckart K, Spiess J (2002) Priming of Long-Term Potentiation in Mouse Hippocampus by Corticotropin-Releasing Factor and Acute Stress: Implications for Hippocampus-Dependent Learning. J Neurosci 22: 3788–3794. https://doi.org/10.1523/JNEUROSCI.22-09-03788.2002
- Pollandt S, Liu J, Orozco-Cabal L, Grigoriadis DE, Vale WW, Gallagher JP, Shinnick-Gallagher P (2006) Cocaine withdrawal enhances long-term potentiation induced by corticotropin-releasing factor at central amygdala glutamatergic synapses via CRF1, NMDA receptors and PKA. Eur J Neurosci 24: 1733–1743. https://doi.org/10.1111/j.1460-9568.2006.05049.x