Influence of Chronic Social Stress on the Expression of Genes Associated with Neurotransmitter Systems in the Hypothalamus of Male Mice

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Аннотация

Chronic social stress caused by repeated negative experiences in agonistic interactions induces depressive-like behavior in male mice. The aim of the study was to study changes in the expression of genes encoding proteins involved in the metabolism, reception, and transport of catecholamines, opioids, glutamate, and GABA under the influence of chronic stress. Hypothalamic samples were sequenced using RNA-Seq. It was shown that the expression of the catecholaminergic genes Adra1b, Adrbk1, Comtd1, Ppp1r1b, Sncb, Sncg, and Th in depressed animals is increased, while the expression of the Maoa and Maob genes is reduced. The expression of the opioidergic and cannabinoidergic genes Pdyn, Penk, Pomc, Pnoc, Ogfr, and Faah was upregulated, while that of the Oprk1, Opcml, Ogfrl1, and Cnr1 genes was downregulated. The expression of the glutamatergic genes Grik3, Grik4, Grik5, Grin1, Grm2, and Grm4 was increased, while the expression of the Gria3, Grik1, Grik2, Grin2a, Grin3a, Grm5, Grm8, and Gad2 genes was reduced. The expression of the GABAergic genes Gabre, Gabbr2, and Slc6a11 was higher, while the expression of the Gabra1, Gabra2, Gabra3, Gabrb2, Gabrb3, Gabrg1, Gabrg2, and Slc6a13 genes was lower in depressed animals. The data suggest that gene products that interact with other neurotransmitter systems (Th, Gad2, Gabra1, Gabrg2, Grin1, and Pdyn) may be of interest as potential targets for pharmacological correction of the consequences of social stress.

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Авторлар туралы

I. Kovalenko

FRC Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: koir0909@mail.ru
Ресей, Novosibirsk, 630090

A. Galyamina

FRC Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Email: koir0909@mail.ru
Ресей, Novosibirsk, 630090

D. Smagin

FRC Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Email: koir0909@mail.ru
Ресей, Novosibirsk, 630090

N. Kudryavtseva

FRC Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences; Pavlov Institute of Physiology, Russian Academy of Sciences

Email: koir0909@mail.ru
Ресей, Novosibirsk, 630090; Saint-Petersburg, 199034

Әдебиет тізімі

  1. Kudryavtseva N.N., Bakshtanovskaya I.V., Koryakina L.A. Social model of depression in mice of C57BL/6J strain // Pharmacol. Biochem. Behav. 1991. V.38. P. 315–320, https://doi.org/10.1016/0091-3057(91)90284-9
  2. Августинович Д.Ф., Алексеенко О.В., Бакштановская И.В. и др. Динамические изменения серотонергической и дофаминергической активности мозга в процессе развития тревожной депрессии: экспериментальное исследование // Успехи физиол. наук. 2004. Т. 35. С. 19–40.
  3. Кудрявцева Н.Н., Амстиславская Т.Г., Августинович Д.Ф. и др. Влияние хронического опыта побед и поражений в социальных конфликтах на состояние серотонергической системы головного мозга мышей // Журн. высшей нервной деят. им. И.П. Павлова. 1996. Т. 46. С. 1088–1096.
  4. Amstislavskaya T.G., Kudryavtseva N.N. Effect of repeated experience of victory and defeat in daily agonistic confrontations on brain tryptophan hydroxylase activity // FEBS Lettr. 1997. V. 406. P. 106–108. https://doi.org/10.1016/s0014-5793(97)00252-4
  5. Smagin D., Boyarskikh U., Bondar N. et al. Reduction of serotonergic gene expression in the raphe nuclei of the midbrain under positive fighting experience in male mice // Adv. Biosci. Biotechnol. 2013. V. 4. P. 36–44.
  6. Puglisi-Allegra S., Cabib S. Effects of defeat experiences on dopamine metabolism in different brain areas of the mouse // Aggress. Behav. 1990 .V. 16. P. 271–284. https://doi.org/10.1358/dnp.1998.11.9.863689
  7. Tidey J.W., Miczek K.A. Social defeat stress selectively alters mesocorticolimbic dopamine release: An in vivo microdialysis study // Brain. Res. 1996. V. 721. P. 140–149. https://doi.org/10.1016/0006-8993(96)00159-x
  8. Fatemi S.H., Stary J.M., Earle J.A. et al. GABAergic dysfunction in schizophrenia and mood disorders as reflected by decreased levels of glutamic acid decarboxylase 65 and 67 kDa and Reelin proteins in cerebellum // Schizophr. Res. 2005. V. 72. P. 109–122. https://doi.org/10.1016/j.schres.2004.02.017
  9. Karolewicz B., Maciag D., O’Dwyer G. et al. Reduced level of glutamic acid decarboxylase 67 kDa in the prefrontal cortex in major depression // Int. J. Neuropsychopharmacol. 2010. V. 13. P. 411–420. https://doi.org/10.1017/S1461145709990587
  10. Browne C.A., Lucki I. Targeting opioid dysregulation in depression for the development of novel therapeutics // Pharmacol. Ther. 2019. V. 201. P. 51–76. https://doi.org/10.1016/j.pharmthera.2019.04.009
  11. Anderson S.A., Michaelides M., Zarnegar P. et al. Impaired periamygdaloid-cortex prodynorphin is characteristic of opiate addiction and depression // J. Clin. Invest. 2013. V. 123. P. 5334–5341. h ttps://doi.org/10.1172/JCI70395
  12. Melo I., Drews E., Zimmer A., Bilkei-Gorzo A. Enkephalin knockout male mice are resistant to chronic mild stress // Genes Brain Behav. 2014. V. 13. P. 550–558. https://doi.org/10.1111/gbb.12139
  13. Qu N., He Y., Wang C. et al. A POMC-originated circuit regulates stress-induced hypophagia, depression, and anhedonia // Mol. Psychiatry. 2020. V. 25. P. 1006–1021. https://doi.org/10.1038/s41380-019-0506-1
  14. Parsons C.G., Danysz W., Quack G. Glutamate in CNS disorders as a target for drug development: an update // Drug. News. Perspect. 1998. V. 11. P. 523–569. https://doi.org/10.1358/dnp.1998.11.9.863689
  15. Nestler E.J., Carlezon W.A. Jr. The mesolimbic dopamine reward circuit in depression // Biol. Psychiatry. 2006. V. 59. P. 1151–1159. https://doi.org/10.1016/j.biopsych.2005.09.018
  16. Hashimoto K. Emerging role of glutamate in the pathophysiology of major depressive disorder // Brain. Res. Rev. 2009. V. 61. P. 105–123. https://doi.org/10.1016/j.brainresrev.2009.05.005
  17. Barker D.J., Root D.H., Zhang S., Morales M. Multiplexed neurochemical signaling by neurons of the ventral tegmental area // J. Chem. Neuroanat. 2016. V. 73. P. 33–42. https://doi.org/10.1016/j.jchemneu.2015.12.016
  18. Kudryavtseva N.N., Smagin D.A., Kovalenko I.L., Vishnivetskaya G.B. Repeated positive fighting experience in male inbred mice // Nat. Protoc. 2014. V. 9. P. 2705–2717. https://doi.org/10.1038/nprot.2014.156
  19. Kudryavtseva N.N., Avgustinovich D.F. Behavioral and physiological markers of experimental depression induced by social conflicts (DISC) // Aggress. Behav. 1998. V. 24. P. 271–286.
  20. Kudryavtseva N.N. Development of mixed anxiety/depression-like state as a consequence of chronic anxiety: Review of experimental data // Curr. Top. Behav. Neurosci. 2022. V. 54. P. 125–152. https://doi.org/10.1007/7854_2021_248
  21. Коваленко И.Л., Смагин Д.А., Галямина А.Г. и др. Изменение экспрессии дофаминергических генов в структурах мозга самцов мышей под влиянием хронического социального стресса: данные RNA-seq // Мол. биология. 2016. V. 50. P. 184–187. https://doi.org/10.7868/S00268984116010080
  22. Hebert M.A., Serova L.I., Sabban E.L. Single and repeated immobilization stress differentially trigger induction and phosphorylation of several transcription factors and mitogenactivated protein kinasesin the rat locus coeruleus // J. Neurochem. 2005. V. 95. P. 484–498. https://doi.org/10.1111/j.1471-4159.2005.03386.x
  23. Kvetnansky R., Sabban E.L., Palkovits M. Catecholaminergic systems in stress: Structural and molecular genetic approaches // Physiol. Rev. 2009. V. 89. P. 535–606. https://doi.org/10.1152/physrev.00042.2006
  24. Kudryavtseva N.N., Smagin D.A., Kovalenko I.L. et al. Serotonergic genes in the development of anxiety/depression-like state and pathology of aggressive behavior in male mice: RNA-seq data // Mol. Biol. 2017. V. 51. P. 251–262, https://doi.org/10.7868/S0026898417020136
  25. George J.M. The synucleins // Genome Biol. 2002. V. 3. https://doi.org/10.1186/gb-2001-3-1-reviews3002
  26. Oaks A.W., Sidhu A. Synuclein modulation of monoamine transporters // FEBS Lett. 2011. V. 585. P. 1001–1006. https://doi.org/10.1016/j.febslet.2011.03.009
  27. Galyamina A.G., Kovalenko I.L., Smagin D.A., Kudryavtseva N.N. Changes in the expression of neurotransmitter system genes in the ventral tegmental area in depressed mice: RNA-seq data // Neurosci. and Behav. Physiol. 2018. V. 48. P. 591–602.
  28. Frieling H., Gozner A., Römer K.D. et al. Alpha-synuclein mRNA levels correspond to beck depression inventory scores in females with eating disorders // Neuropsychobiology. 2008. V. 58. P. 48–52. https://doi.org/10.1159/000155991
  29. Ninkina N., Peters O., Millership S. et al. Gamma-synucleinopathy: Neurodegeneration associated with overexpression of the mouse protein // Hum. Mol. Genet. 2009. V. 18. P. 1779–1794. https://doi.org/10.1093/hmg/ddp090
  30. Merrill J.O., Korff M., Banta-Green C.J. et. al. Prescribed opioid difficulties, depression and opioid dose among chronic opioid therapy patients // Gen. Hosp. Psychiatry. 2012. V. 34. P. 581–587. https://doi.org/10.1016/j.genhosppsych.2012.06.018
  31. Scherrer J. F., Salas J., Copeland L.A. et al. Prescription opioid duration, dose, and increased risk of depression in 3 large patient populations //Ann. Fam. Med. 2016. V. 14. P. 54–62. https://doi.org/10.1370/afm.1885
  32. Lazary J., Eszlari N., Juhasz G., Bagdy G. Genetically reduced FAAH activity may be a risk for the development of anxiety and depression in persons with repetitive childhood trauma // Eur. Neuropsychopharmacol. 2016. V. 26. P. 1020–1028. https://doi.org/10.1016/j.euroneuro.2016.03.003
  33. Wang Y., Zhang X. FAAH inhibition produces antidepressant-like efforts of mice to acute stress via synaptic long-term depression // Behav. Brain Res. 2017. V. 324. P. 138–145. https://doi.org/10.1016/j.bbr.2017.01.054
  34. Domschke K., Dannlowski U., Ohrmann P. et al. Cannabinoid receptor 1 (CNR1) gene: Impact on antidepressant treatment response and emotion processing in major depression // Eur. Neuropsychopharmacol. 2008. V. 18. P. 751–759. https://doi.org/10.1016/j.euroneuro.2008.05.003
  35. Mitjans M., Serretti A., Fabbri C. et al. Screening genetic variability at the CNR1 gene in both major depression etiology and clinical response to citalopram treatment // Psychopharmacology. 2013. V. 227. P. 509–519, https://doi.org/10.1007/s00213-013-2995-y
  36. Masih J., Verbeke W. Exploring association of opioid receptor genes polymorphism with positive and negative moods using Positive and Negative Affective States Scale (PANAS) // Clin. Exp. Psychol. 2019. V. 5. № 1. P. 1–6.
  37. Schol-Gelok S., Janssens A. C., Tiemeier, H. et al. A genome-wide screen for depression in two independent Dutch populations // Biol. Psychiatry. 2010. V. 68. P. 187–196. https://doi.org/10.1016/j.biopsych.2010.01.033
  38. Li X., Tizzano J.P., Griffey K. et al. Antidepressant-like actions of an AMPA receptor potentiator (LY392098) // Neuropharmacology. 2001. V. 40. P. 1028–1033. https://doi.org/10.1016/s0028-3908(00)00194-5
  39. Kotlinska J., Liljequist S. The putative AMPA receptor antagonist, LY326325, produces anxiolytic effects without altering locomotor activity in rats // Pharmacol. Biochem. Behav. 1998. V. 60. P. 119–124. https://doi.org/10.1016/s0091-3057(97)00565-0
  40. Walker D.L., Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction // Pharmacol. Biochem. Behav. 2002. V.71. P. 379–392. https://doi.org/10.1016/s0091-3057(01)00698-0
  41. Chourbaji S., Vogt M.A., Fumagalli F. et al. AMPA receptor subunit 1 (GluRA) knockout mice model the glutamate hypothesis of depression // FASEB J. 2008. V. 22. P. 3129–3134. https://doi.org/10.1096/fj.08-106450
  42. Papp M., Moryl E. Antidepressant activity of non-competitive and competitive NMDA receptor antagonists in a chronic mild stress model of depression // Eur. J. Pharmacol. 1994. V. 263. P. 1–7. https://doi.org/10.1016/0014-2999(94)90516-9
  43. Wiley J.L., Cristello A.F., Balster R.L. Effects of site-selective NMDA receptor antagonists in an elevated plus-maze model of anxiety in mice // Eur. J. Pharmacol. 1995. V. 294. P. 101–107. https://doi.org/10.1016/0014-2999(95)00506-4
  44. Barkus C., McHugh S.B., Sprengel R. et al. Hippocampal NMDA receptors and anxiety: At the interface between cognition and emotion // Eur. J. Pharmacol. 2010. V. 626. P. 49–56. https://doi.org/10.1016/j.ejphar.2009.10.014
  45. Stelly C.E., Pomrenze M.B., Cook J.B., Morikawa H. Repeated social defeat stress enhances glutamatergic synaptic plasticity in the VTA and cocaine place conditioning // Elife. 2016. V. 5. https://doi.org/10.7554/eLife.15448
  46. Wieronska J.M., Branski P., Szewczyk B. et al. Changes in the expression of metabotropic glutamate receptor 5 (mGluR5) in the rat hippocampus in an animal model of depression // Pol. J. Pharmacol. 2001. V. 53. P. 659–662.
  47. Wang H., Zhu Y.Z., Wong P. T.-H. et al. cDNA microarray analysis of gene expression in anxious PVG and SD rats after cat-freezing test. // Exp. Brain. Res. 2003. V. 149. P. 413–421. https://doi.org/10.1007/s00221-002-1369-1
  48. Kroes R.A., Panksepp J., Burgdorf J. et al. Modeling depression: Social dominance-submission gene expression patterns in rat neocortex // Neuroscience. 2006. V. 137. P. 37–49. https://doi.org/10.1016/j.neuroscience.2005.08.076
  49. Tanay V.A., Glencorse T.A., Greenshaw A.J. et al.. Chronic administration of antipanic drugs alters rat brainstem GABAA receptor subunit mRNA levels // Neuropharmacology. 1996. V. 35. P. 1475–1482. https://doi.org/10.1016/s0028-3908(96)00065-2
  50. Tanay V.M., Greenshaw A.J., Baker G.B., Bateson A.N. Common effects of chronically administered antipanic drugs on brainstem GABA(A) receptor subunit gene expression // Mol. Psychiatry. 2001. V. 6. P. 404–412. https://doi.org/10.1038/sj.mp.4000879
  51. Ménard C., Tse Y.C., Cavanagh C. et al. Knockdown of prodynorphin gene prevents cognitive decline, reduces anxiety, and rescues loss of group 1 metabotropic glutamate receptor function in aging // J. Neurosci. 2013. V. 33. P. 12792–12804. https://doi.org/10.1523/JNEUROSCI.0290-13.2013
  52. Ménard C., Quirion R., Bouchard S. et al. Glutamatergic signaling and low prodynorphin expression are associated with intact memory and reduced anxiety in rat models of healthy aging // Front. Aging Neurosci. 2014. V. 6. https://doi.org/10.3389/fnagi.2014.00081
  53. Smagin D.A., Kovalenko I.L., Galyamina A.G. et al. Dysfunction in ribosomal gene expression in the hypotalamus and hippocampus following chronic social defeat stress in male mice as revealed by RNA-seq // Neural. Plast. 2016. 3289187.
  54. Raimundo N. Mitochondrial pathology: Stress signals from the energy factory // Trends in Molecular Medicine. 2014. V. 20. N. 5. P. 282–292.
  55. Кудрявцева Н.Н., Шурлыгина А.В., Галямина А.Г. и др. Иммунопатология смешанного тревожно-депрессивного расстройства: экспериментальный подход к коррекции иммунодефицитных состояний // Журн. высшей нервной деят. им И.П. Павлова. 2017. Т. 67. № 6. С. 671–692.

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2. Fig. 1. Expression of DEG of catecholaminergic systems in GPT in depressed male mice. White columns are control, dark columns are depressive mice. * p < 0.05, ** p < 0.01, *** p < 0.001 vs. control. An auxiliary scale is presented for the Sncb gene. The data is expressed in FPKM units. # – previously published data [21].

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3. Fig. 2. Expression of DEG opioidergic and cannabinoid systems in GPT in depressed male mice. White columns are control, dark columns are depressive mice. *p < 0.05, ** p < 0.01, *** p < 0.001 vs. control. The data is expressed in FPKM units.

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4. Fig. 3. Expression of the DEG glutamatergic system in GPT in depressed male mice. White columns are control, dark columns are depressive mice. *p < 0.05, **p < 0.01, ***p < 0.001 vs. control. An auxiliary scale is presented for the Gad2, Grik5, and Grin1 genes. The data is expressed in FPKM units.

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5. Fig. 4. Expression of the DEG GABAergic system in GPT in depressed male mice. White columns are control, dark columns are depressive mice. *p < 0.05, **p < 0.01, ***p < 0.001 vs. control. An auxiliary scale is presented for the Slc6a11 gene. The data is expressed in FPKM units.

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6. Fig. 5. Functional relationships of proteins encoded by DEG, established according to the STRING database (http://string-db.org /) in depressed animals in GPT.

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