Deletion of the clock gene Period2 (Per2) in glial cells alters mood-related behavior in mice.

Tytuł:: Deletion of the clock gene Period2 (Per2) in glial cells alters mood-related behavior in mice.
Autorzy:: Martini T; Department of Biology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland.
Ripperger JA; Department of Biology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland.
Stalin J; Department of Oncology, Microbiology and Immunology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland.
Kores A; Department of Biology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland.
Stumpe M; Department of Biology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland.
Albrecht U; Department of Biology, Faculty of Science and Medicine, University of Fribourg, 1700, Fribourg, Switzerland. .
Źródło:: Scientific reports [Sci Rep] 2021 Jun 10; Vol. 11 (1), pp. 12242. Date of Electronic Publication: 2021 Jun 10.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: London : Nature Publishing Group, copyright 2011-
MeSH Terms:: Affect*
Behavior, Animal*
Sequence Deletion*
Neuroglia/*metabolism
Period Circadian Proteins/*genetics
Animals ; Astrocytes/metabolism ; Breeding ; Circadian Rhythm ; Dependovirus/genetics ; Gene Expression ; Genetic Association Studies ; Genetic Vectors/genetics ; Mice ; Phenotype ; Transduction, Genetic
References:: Abarca, C., Albrecht, U. & Spanagel, R. Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl. Acad. Sci. U S A 99, 9026–9030 (2002). (PMID: 1208494012441710.1073/pnas.142039099)
Albrecht, U. & Ripperger, J. A. Circadian clocks and sleep: impact of rhythmic metabolism and waste clearance on the brain. Trends Neurosci. 41, 677–688 (2018). (PMID: 3027460310.1016/j.tins.2018.07.007)
Alexander, L. et al. Over-activation of primate subgenual cingulate cortex enhances the cardiovascular, behavioral and neural responses to threat. Nat. Commun. 11, 5386 (2020). (PMID: 33106488758841210.1038/s41467-020-19167-0)
Altshuler, L. L. et al. Amygdala astrocyte reduction in subjects with major depressive disorder but not bipolar disorder. Bipolar. Disord. 12, 541–549 (2010). (PMID: 2071275610.1111/j.1399-5618.2010.00838.x)
Banasr, M. & Duman, R. S. Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol. Psychiatr. 64, 863–870 (2008). (PMID: 10.1016/j.biopsych.2008.06.008)
Barca-Mayo, O. et al. Astrocyte deletion of Bmal1 alters daily locomotor activity and cognitive functions via GABA signalling. Nat. Commun. 8, 14336 (2017). (PMID: 28186121530980910.1038/ncomms14336)
Bhagwagar, Z. et al. Low GABA concentrations in occipital cortex and anterior cingulate cortex in medication-free, recovered depressed patients. Int. J. Neuropsychopharmacol. 11, 255–260 (2008). (PMID: 1762502510.1017/S1461145707007924)
Brancaccio, M. et al. Cell-autonomous clock of astrocytes drives circadian behavior in mammals. Science 363, 187–192 (2019). (PMID: 30630934644065010.1126/science.aat4104)
Brenna, A. et al. Cyclin-dependent kinase 5 (CDK5) regulates the circadian clock. Elife 8, 10 (2019). (PMID: 10.7554/eLife.50925)
Challis, R. C. et al. Systemic AAV vectors for widespread and targeted gene delivery in rodents. Nat. Protoc. 14, 379–414 (2019). (PMID: 3062696310.1038/s41596-018-0097-3)
Chan, K. Y. et al. Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat. Neurosci. 20, 1172–1179 (2017). (PMID: 28671695552924510.1038/nn.4593)
Chappuis, S. et al. Role of the circadian clock gene Per2 in adaptation to cold temperature. Mol. Met. 2, 184–193 (2013). (PMID: 10.1016/j.molmet.2013.05.002)
Chavan, R. et al. Liver-derived ketone bodies are necessary for food anticipation. Nat. Commun. 7, 10580 (2016). (PMID: 26838474474285510.1038/ncomms10580)
Choudary, P. V. et al. Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc. Natl. Acad. Sci. U S A 102, 15653–15658 (2005). (PMID: 16230605125739310.1073/pnas.0507901102)
Chung, S. et al. Impact of circadian nuclear receptor REV-ERBalpha on midbrain dopamine production and mood regulation. Cell 157, 858–868 (2014). (PMID: 2481360910.1016/j.cell.2014.03.039)
Cipriani, A. et al. 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 (2018). (PMID: 29477251588978810.1016/S0140-6736(17)32802-7)
Davis, M. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15, 353–375 (1992). (PMID: 157544710.1146/annurev.ne.15.030192.002033)
Dibner, C., Schibler, U. & Albrecht, U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517–549 (2010). (PMID: 2014868710.1146/annurev-physiol-021909-135821)
Duncan, G. E., Johnson, K. B. & Breese, G. R. Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity. J. Neurosci. 13, 3932–3943 (1993). (PMID: 8366353657645410.1523/JNEUROSCI.13-09-03932.1993)
Etievant, A. et al. Astroglial control of the antidepressant-like effects of prefrontal cortex deep brain stimulation. EBioMedicine 2, 898–908 (2015). (PMID: 26425697456313810.1016/j.ebiom.2015.06.023)
Gadea, A. & Lopez-Colome, A. M. Glial transporters for glutamate, glycine, and GABA: II. GABA transporters. J. Neurosci. Res. 63, 461–468 (2001). (PMID: 1124158110.1002/jnr.1040)
GBD. Disease and Injury Incidence and Prevalence Collaborators (2018). Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392, 1789–1858 (2017).
Hampp, G. et al. Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr. Biol. 18, 678–683 (2008). (PMID: 1843982610.1016/j.cub.2008.04.012)
Harno, E., Cottrell, E. C. & White, A. Metabolic pitfalls of CNS Cre-based technology. Cell Metab. 18, 21–28 (2013). (PMID: 2382347510.1016/j.cmet.2013.05.019)
Ikeda, E. et al. Molecular mechanism regulating 24-hour rhythm of dopamine D3 receptor expression in mouse ventral striatum. Mol. Pharmacol. 83, 959–967 (2013). (PMID: 2342991110.1124/mol.112.083535)
Jackson, F. R., You, S. & Crowe, L. B. Regulation of rhythmic behaviors by astrocytes. Rev. Dev. Biol. 9, 372 (2020).
Jud, C., Schmutz, I., Hampp, G., Oster, H. & Albrecht, U. A guideline for analyzing circadian wheel-running behavior in rodents under different lighting conditions. Biol. Proced. Online 7, 101–116 (2005). (PMID: 16136228119038110.1251/bpo109)
Li, J. Z. et al. Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc. Natl. Acad. Sci. U S A 110, 9950–9955 (2013). (PMID: 23671070368371610.1073/pnas.1305814110)
Lindhorst, A., Bechmann, I. & Gericke, M. Unspecific DNA recombination in AdipoqCre-ER(T2)-mediated knockout approaches in transgenic mice is sex-, age- and genotype-dependent. Adipocyte 9, 1–6 (2020). (PMID: 3184267010.1080/21623945.2019.1701394)
Luo, L. et al. Optimizing nervous system-specific gene targeting with cre driver lines: prevalence of germline recombination and influencing factors. Neuron 106, 37–65 (2020). (PMID: 32027825737738710.1016/j.neuron.2020.01.008)
Luscher, B., Shen, Q. & Sahir, N. The GABAergic deficit hypothesis of major depressive disorder. Mol. Psychiatr. 16, 383–406 (2011). (PMID: 10.1038/mp.2010.120)
Magistretti, P. J. Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304–2311 (2006). (PMID: 1673180610.1242/jeb.02208)
Martini, T., Ripperger, J. A. & Albrecht, U. Measuring food anticipation in mice. Clocks Sleep 1, 65–74 (2019). (PMID: 3138475110.3390/clockssleep1010007)
McClung, C. A. et al. Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc. Natl. Acad. Sci. U S A 102, 9377–9381 (2005). (PMID: 15967985116662110.1073/pnas.0503584102)
Miyazaki, J. et al. Expression vector system based on the chicken beta-actin promoter directs efficient production of interleukin-5. Gene 79, 269–277 (1989). (PMID: 255177810.1016/0378-1119(89)90209-6)
Nestler, E. J. & Carlezon, W. A. Jr. The mesolimbic dopamine reward circuit in depression. Biol. Psychiatr. 59, 1151–1159 (2006). (PMID: 10.1016/j.biopsych.2005.09.018)
Pariante, C. M. & Lightman, S. L. The HPA axis in major depression: classical theories and new developments. Trends Neurosci. 31, 464–468 (2008). (PMID: 1867546910.1016/j.tins.2008.06.006)
Partonen, T. et al. Three circadian clock genes Per2, Arntl, and Npas2 contribute to winter depression. Annu. Med. 39, 229–238 (2007). (PMID: 10.1080/07853890701278795)
Porsolt, R. D., Anton, G., Blavet, N. & Jalfre, M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 47, 379–391 (1978). (PMID: 20449910.1016/0014-2999(78)90118-8)
Quintana, A. et al. Lack of GPR88 enhances medium spiny neuron activity and alters motor- and cue-dependent behaviors. Nat. Neurosci. 15, 1547–1555 (2012). (PMID: 23064379348341810.1038/nn.3239)
Rodriguez-Romaguera, J. et al. Prepronociceptin-expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli. Cell Rep. 33, 108362 (2020). (PMID: 33176134813628510.1016/j.celrep.2020.108362)
Rosbash, M. The implications of multiple circadian clock origins. PLoS Biol. 7, e62 (2009). (PMID: 1929672310.1371/journal.pbio.1000062)
Rubio, F. J., Li, X., Liu, Q. R., Cimbro, R. & Hope, B. T. Fluorescence activated cell sorting (FACS) and gene expression analysis of fos-expressing neurons from fresh and frozen rat brain tissue. J. Vis. Exp. 114, 54358 (2016).
Schmutz, I., Ripperger, J. A., Baeriswyl-Aebischer, S. & Albrecht, U. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev. 24, 345–357 (2010). (PMID: 20159955281673410.1101/gad.564110)
Schwarz, J. M., Smith, S. H. & Bilbo, S. D. FACS analysis of neuronal-glial interactions in the nucleus accumbens following morphine administration. Psychopharmacology 230, 525–535 (2013). (PMID: 23793269413401110.1007/s00213-013-3180-z)
Song, A. J. & Palmiter, R. D. Detecting and avoiding problems when using the cre-lox system. Trends Genet 34, 333–340 (2018). (PMID: 29336844591017510.1016/j.tig.2017.12.008)
Spanagel, R. et al. The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat. Med. 11, 35–42 (2005). (PMID: 1560865010.1038/nm1163)
Takahashi, J. S. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 18, 164–179 (2017). (PMID: 2799001910.1038/nrg.2016.150)
Tso, C. F. et al. Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr. Biol. 27, 1055–1061 (2017). (PMID: 28343966538059210.1016/j.cub.2017.02.037)
Zhang, L. et al. A PERIOD3 variant causes a circadian phenotype and is associated with a seasonal mood trait. Proc. Natl. Acad. Sci. U S A 113, E1536–E1544 (2016). (PMID: 269036304801303)
Zheng, B. et al. The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400, 169–173 (1999). (PMID: 1040844410.1038/22118)
Zhou, X. et al. Astrocyte, a promising target for mood disorder interventions. Front Mol. Neurosci. 12, 136 (2019). (PMID: 31231189656015610.3389/fnmol.2019.00136)
Zhuo, L. et al. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31, 85–94 (2001). (PMID: 1166868310.1002/gene.10008)
Zink, M., Vollmayr, B., Gebicke-Haerter, P. J. & Henn, F. A. Reduced expression of GABA transporter GAT3 in helpless rats, an animal model of depression. Neurochem. Res. 34, 1584–1593 (2009). (PMID: 1928827510.1007/s11064-009-9947-2)
Substance Nomenclature:: 0 (Per2 protein, mouse)
0 (Period Circadian Proteins)
Entry Date(s):: Date Created: 20210611 Date Completed: 20211027 Latest Revision: 20230203
Update Code:: 20240104
PubMed Central ID:: PMC8192521
DOI:: 10.1038/s41598-021-91770-7
PMID:: 34112905
: Czasopismo naukowe

Pełny tekst

The circadian clock regulates many biochemical and physiological pathways, and lack of clock genes, such as Period (Per) 2, affects not only circadian activity rhythms, but can also modulate feeding and mood-related behaviors. However, it is not known how cell-type specific expression of Per2 contributes to these behaviors. In this study, we find that Per2 in glial cells is important for balancing mood-related behaviors, without affecting circadian activity parameters. Genetic and adeno-associated virus-mediated deletion of Per2 in glial cells of mice leads to reduced despair and anxiety. This is paralleled by an increase of the GABA transporter 2 (Gat2/Slc6a13) and Dopamine receptor D3 (Drd3) mRNA, and a reduction of glutamate levels in the nucleus accumbens (NAc). Interestingly, neuronal Per2 knock-out also reduces despair, but does not influence anxiety. The change in mood-related behavior is not a result of a defective molecular clock, as glial Bmal1 deletion has no effect on neither despair nor anxiety. Exclusive deletion of Per2 in glia of the NAc reduced despair, but had no influence on anxiety. Our data provide strong evidence for an important role of glial Per2 in regulating mood-related behavior.

Zaloguj się, aby uzyskać dostęp do pełnego tekstu.

Informacja