Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Strain Differences in the Chronic Mild Stress Animal Model of Depression and Anxiety in Mice

  • Jung, Yang-Hee (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Hong, Sa-Ik (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Ma, Shi-Xun (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Hwang, Ji-Young (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Kim, Jun-Sup (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Lee, Ju-Hyun (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Seo, Jee-Yeon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Lee, Seok-Yong (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University) ;
  • Jang, Choon-Gon (Department of Pharmacology, School of Pharmacy, Sungkyunkwan University)
  • Received : 2014.05.20
  • Accepted : 2014.06.24
  • Published : 2014.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Chronic mild stress (CMS) has been reported to induce an anhedonic-like state in mice that resembles some of the symptoms of human depression. In the present study, we used a chronic mild stress animal model of depression and anxiety to examine the responses of two strains of mice that have different behavioral responsiveness. An outbred ICR and an inbred C57BL/6 strain of mice were selected because they are widely used strains in behavioral tests. The results showed that the inbred C57BL/6 and outbred ICR mice were similarly responsive to CMS treatment in sucrose intake test (SIT) and open field test (OFT). However, the two strains showed quite different responses in forced swimming test (FST) and novelty-suppressed feeding (NSF) test after 3 weeks of CMS treatment. Only C57BL/6 mice displayed the depression- and anxiety-like behavioral effects in response to CMS treatment in FST and NSF test. Our results suggest that there are differences in responsiveness to CMS according to the different types of strain of mice and behavioral tests. Therefore, these results provide useful information for the selection of appropriate behavioral methods to test depression- and anxiety-like behaviors using CMS in ICR and C57BL/6 mice.

Keywords

References

  1. Bekris, S., Antoniou, K., Daskas, S. and Papadopoulou-Daifoti, Z. (2005) Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains. Behav. Brain Res. 161, 45-59. https://doi.org/10.1016/j.bbr.2005.01.005
  2. Bessa, J. M., Mesquita, A. R., Oliveira, M., Pego, J. M. Cerqueira, J. J., Palha, J. A., Almeida, O. F. and Sousa, N. (2009) A transdimensional approach to the behavioral aspects of depression. Front. Behav. Neurosci. 3, 1.
  3. Bodnoff, S. R., Suranyi-Cadotte, B., Aitken, D. H., Quirion, R., Meaney and M. J. (1988) The effects of chronic antidepressant treatment in an animal model of anxiety. Psychopharmacology 95, 298-302.
  4. Briones, A., Gagno, S., Martisova, E., Dobarro, M., Aisa, B., Solas, M., Tordera, R. and Ramirez, M. (2012) Stress-induced anhedonia is associated with an increase in Alzheimer's disease-related markers. Br. J. Pharmacol. 165, 897-907. https://doi.org/10.1111/j.1476-5381.2011.01602.x
  5. Elizalde, N., Garcia-Garcia, A. L., Totterdell, S., Gendive, N., Venzala, E., Ramirez, M. J., Del Rio, J. and Tordera, R. M. (2010) Sustained stress-induced changes in mice as a model for chronic depression. Psychopharmacology 210, 393-406. https://doi.org/10.1007/s00213-010-1835-6
  6. Grivas, V., Markou, A. and Pitsikas, N. (2013) The metabotropic glutamate 2/3 receptor agonist LY379268 induces anxiety-like behavior at the highest dose tested in two rat models of anxiety. Eur. J. Pharmacol. 715, 105-110. https://doi.org/10.1016/j.ejphar.2013.05.048
  7. Gronli, J., Murison, R., Fiske, E., Bjorvatn, B., Sorensen, E., Portas, C.M. and Ursin, R. (2005) Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84, 571-577. https://doi.org/10.1016/j.physbeh.2005.02.007
  8. Jang, C. G., Whitfield, T., Schulteis, G., Koob, G. F. and Wee, S. (2013) A dysphoric-like state during early withdrawal from extended access to methamphetamine self-administration in rats. Psychopharmacology 225, 753-763. https://doi.org/10.1007/s00213-012-2864-0
  9. Kaufman, J. and Charney, D. (2000) Comorbidity of mood and anxiety disorders. Depress Anxiety 12, 69-76. https://doi.org/10.1002/1520-6394(2000)12:1+<69::AID-DA9>3.0.CO;2-K
  10. Kendler, K. S., Karkowski, L. M. and Prescott, C. A. (1999) Causal relationship between stressful life events and the onset of major depression. Am. J. Psychiatry 156, 837-841. https://doi.org/10.1176/ajp.156.6.837
  11. Kessler, R. C. (1997) The effects of stressful life events on depression. Annu. Rev. Psychol. 48, 191-214 https://doi.org/10.1146/annurev.psych.48.1.191
  12. Kim, S. J., Lee, M. S., Kim, J. H., Lee, T. H. and Shim, I. (2013) Antidepressant-like effects of Lycii Radicis Cortex and betaine in the forced swimming test in rats. Biomol. Ther. 21, 79-83. https://doi.org/10.4062/biomolther.2012.072
  13. Lee, B., Sur, B., Kwon, S., Yeom, M., Shim, I., Lee, H. and Hahm, D. H. (2013) Chronic administration of catechin decreases depression and anxiety-like behaviors in a rat model using chronic corticosterone injections. Biomol. Ther. 21, 313-322. https://doi.org/10.4062/biomolther.2013.004
  14. Li, S., Wang, C., Wang, W., Dong, H., Hou, P. and Tang, Y. (2008) Chronic mild stress impairs cognition in mice: From brain homeostasis to behavior. Life Sci. 82, 934-942. https://doi.org/10.1016/j.lfs.2008.02.010
  15. Liu, X. and Gershenfeld, H. K. (2001) Genetic differences in the tailsuspension test and its relationship to imipramine response among 11 inbred strains of mice. Biol. Psychiatry 49, 575-581. https://doi.org/10.1016/S0006-3223(00)01028-3
  16. Lucki, I., Dalvi, A. and Mayorga, A. J. (2001) Sensitivity to the effects of pharmacologically selective antidepressants in different strains of mice. Psychopharmacology 155, 315-322. https://doi.org/10.1007/s002130100694
  17. Ma, X. C., Jiang, D., Jiang, W. H., Wang, F., Jia, M., Wu, J., Hashimoto, K., Dang, Y. H. and Gao, Cg. (2011) Social isolation-induced aggression potentiates anxiety and depressive-like behavior in male mice subjected to unpredictable chronic mild stress. PLoS ONE 6, e20955 https://doi.org/10.1371/journal.pone.0020955
  18. Matthews, K., Forbes, N. and Reid, I. C. (1995) Sucrose consumption as an hedonic measure following chronic unpredictable mild stress. Physiol. Behav. 57, 241-248. https://doi.org/10.1016/0031-9384(94)00286-E
  19. Mayorga, A. J. and Lucki, I. (2001) Limitations on the use of the C57BL/6 mouse in the tail suspension test. Psychopharmacology 155, 110-112. https://doi.org/10.1007/s002130100687
  20. Mineur, Y. S., Belzung, C. and Crusio, W. E. (2006) Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. 175, 43-50. https://doi.org/10.1016/j.bbr.2006.07.029
  21. Mineur, Y. S., Prasol, D. J., Belzung, C. and Crusio, W. E. (2003) Agonistic behavior and unpredictable chronic mild stress in mice. Behav. Genet. 33, 513-519. https://doi.org/10.1023/A:1025770616068
  22. Porsolt, R. D., Le Pichon, M. and Jalfre, M. (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266, 730-732. https://doi.org/10.1038/266730a0
  23. Pothion, S., Bizot, J. C., Trovero, F. and Belzung, C. (2004) Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 155, 135-146. https://doi.org/10.1016/j.bbr.2004.04.008
  24. Prut, L. and Belzung, C. (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. Eur. J. Pharmacol. 463, 3-33. https://doi.org/10.1016/S0014-2999(03)01272-X
  25. Sakata, K., Jin, L. and Jha, S. (2010) Lack of promoter IV-driven BDNF transcription results in depression-like behavior. Genes Brain Behav. 9, 712-721. https://doi.org/10.1111/j.1601-183X.2010.00605.x
  26. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C. and Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. https://doi.org/10.1126/science.1083328
  27. Schweizer, M. C., Henniger, M. S. H. and Sillaber, I. (2009) Chronic mild stress (CMS) in mice: Of anhedonia, 'anomalous anxiolysis' and activity. PLoS ONE 4, e4326 https://doi.org/10.1371/journal.pone.0004326
  28. Stedenfeld, K. A., Clinton, S. M., Kerman, I. A., Akil, H., Watson, S. J. and Sved, A. F. (2011) Novelty-seeking behavior predicts vulnerability in a rodent model of depression. Physiol. Behav. 103, 210-216. https://doi.org/10.1016/j.physbeh.2011.02.001
  29. Strekalova, T., Spanagel, R., Bartsch, D., Henn, F. A. and Gass, P. (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29, 2007-2017. https://doi.org/10.1038/sj.npp.1300532
  30. Willner, P. (1997) Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology 134, 319-329. https://doi.org/10.1007/s002130050456
  31. Willner, P. (2005) Chronic mild stress (CMS) revisited: Consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52, 90-110. https://doi.org/10.1159/000087097
  32. Willner, P., Muscat, R. and Papp, M. (1992) Chronic mild stress-induced anhedonia: A realistic animal model of depression. Neurosci. Biobehav. Rev. 16, 525-534. https://doi.org/10.1016/S0149-7634(05)80194-0
  33. Wu, H. H. and Wang, S. (2010) Strain differences in the chronic mild stress animal model of depression. Behav. Brain Res. 213, 94-102. https://doi.org/10.1016/j.bbr.2010.04.041
  34. Yalcin, I., Belzung, C. and Surget, A. (2008) Mouse strain differences in the unpredictable chronic mild stress: a four-antidepressant survey. Behav. Brain Res. 193, 140-143. https://doi.org/10.1016/j.bbr.2008.04.021
  35. Zhang, K., Song, X., Xu, Y., Li, X., Liu, P., Sun, N., Zhao, X., Liu, Z., Xie, Z. and Peng, J. (2013) Continuous GSK-3${\beta}$ overexpression in the hippocampal dentate gyrus induces prodepressant-like effects and increases sensitivity to chronic mild stress in mice. J. Affect. Disord. 146, 45-52. https://doi.org/10.1016/j.jad.2012.08.033
  36. Zhu, X. H., Yan, H. C., Zhang, J., Qu, H. D., Qiu, X. S., Chen, L., Li, S. J., Cao, X., Bean, J. C., Chen, L. H., Qin, X. H., Liu, J. H., Bai, X. C., Mei, L. and Gao, T. M. (2010) Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J. Neurosci. 30, 12653-12663. https://doi.org/10.1523/JNEUROSCI.6414-09.2010

Cited by

  1. The role of allopregnanolone in the anxiolytic-like effect of free and easy wanderer plus (FEWP), a polyherbal preparation vol.595, 2015, https://doi.org/10.1016/j.neulet.2015.03.039
  2. Therapeutic implications of the choroid plexus–cerebrospinal fluid interface in neuropsychiatric disorders vol.50, 2015, https://doi.org/10.1016/j.bbi.2015.06.010
  3. The hippocampal transcriptomic signature of stress resilience in mice with microglial fractalkine receptor (CX3CR1) deficiency vol.61, 2017, https://doi.org/10.1016/j.bbi.2016.11.023
  4. Pathogenesis of depression: Insights from human and rodent studies vol.321, 2016, https://doi.org/10.1016/j.neuroscience.2015.05.053
  5. Two standardized fractions of Gardenia jasminoides Ellis with rapid antidepressant effects are differentially associated with BDNF up-regulation in the hippocampus vol.187, 2016, https://doi.org/10.1016/j.jep.2016.04.023
  6. Intravenous transplantation of mouse embryonic stem cells attenuates demyelination in an ICR outbred mouse model of demyelinating diseases vol.11, pp.10, 2016, https://doi.org/10.4103/1673-5374.193239
  7. The Unexpected Effects of Beneficial and Adverse Social Experiences during Adolescence on Anxiety and Aggression and Their Modulation by Genotype vol.10, 2016, https://doi.org/10.3389/fnbeh.2016.00097
  8. Chronic mild stress in submissive mice: Marked polydipsia and social avoidance without hedonic deficit in the sucrose preference test vol.298, 2016, https://doi.org/10.1016/j.bbr.2015.10.049
  9. Behavioral effects of chronic stress in the Fmr1 mouse model for fragile X syndrome vol.320, 2017, https://doi.org/10.1016/j.bbr.2016.11.051
  10. Social experiences during adolescence affect anxiety-like behavior but not aggressiveness in male mice vol.326, 2017, https://doi.org/10.1016/j.bbr.2017.03.017
  11. Molecular hydrogen increases resilience to stress in mice vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-10362-6
  12. Effects of stress on behavior and resting-state fMRI in rats and evaluation of Telmisartan therapy in a stress-induced depression model vol.18, pp.1, 2018, https://doi.org/10.1186/s12888-018-1880-y
  13. Hippocampal nuclear factor kappa B accounts for stress-induced anxiety behaviors via enhancing neuronal nitric oxide synthase (nNOS)-carboxy-terminal PDZ ligand of nNOS-Dexras1 coupling vol.146, pp.5, 2018, https://doi.org/10.1111/jnc.14478
  14. Regional alterations of cerebral [18F]FDG metabolism in the chronic unpredictable mild stress- and the repeated corticosterone depression model in rats vol.125, pp.9, 2018, https://doi.org/10.1007/s00702-018-1899-8
  15. On the Developmental Timing of Stress: Delineating Sex-Specific Effects of Stress across Development on Adult Behavior vol.8, pp.7, 2018, https://doi.org/10.3390/brainsci8070121
  16. Involvement of the central hypothalamic-pituitary-adrenal axis in hair growth and melanogenesis among different mouse strains vol.13, pp.10, 2014, https://doi.org/10.1371/journal.pone.0202955
  17. Distinctive stress sensitivity and anxiety-like behavior in female mice: Strain differences matter vol.9, pp.None, 2018, https://doi.org/10.1016/j.ynstr.2018.08.002
  18. Early Blood Profile of C57BL/6 Mice Exposed to Chronic Unpredictable Stress vol.10, pp.None, 2014, https://doi.org/10.3389/fpsyt.2019.00230
  19. Increased expression of plasminogen activator inhibitor-1 (PAI-1) is associated with depression and depressive phenotype in C57Bl/6J mice vol.237, pp.12, 2014, https://doi.org/10.1007/s00221-019-05682-0
  20. Baseline Depression-Like Behaviors in Wild-Type Adolescent Mice Are Strain and Age but Not Sex Dependent vol.15, pp.None, 2014, https://doi.org/10.3389/fnbeh.2021.759574
  21. Methoxphenidine (MXP) induced abnormalities: Addictive and schizophrenia‐related behaviours based on an imbalance of neurochemicals in the brain vol.178, pp.19, 2014, https://doi.org/10.1111/bph.15528
  22. Tianeptine, but not fluoxetine, decreases avoidant behavior in a mouse model of early developmental exposure to fluoxetine vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-02074-9