Cited by 49Stress Responses and CortisolCircadian rhythm and melatoninCancer, Stress, Anesthesia, and Immune Response

Time matters: pathological effects of repeated psychosocial stress during the active, but not inactive, phase of male mice

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Bartlang, Manuela S, Neumann, Inga D, Slattery, David A, Uschold-Schmidt, Nicole, Kraus, Dominik, Helfrich-Förster, Charlotte, Reber, Stefan O·2012·Journal of Endocrinology

Abstract

Recent findings in rats indicated that the physiological consequences of repeated restraint stress are dependent on the time of day of stressor exposure. To investigate whether this is also true for clinically more relevant psychosocial stressors and whether repeated stressor exposure during the light phase or dark phase is more detrimental for an organism, we exposed male C57BL/6 mice to social defeat (SD) across 19 days either in the light phase between Zeitgeber time (ZT)1 and ZT3 (SDL mice) or in the dark phase between ZT13 and ZT15 (SDD mice). While SDL mice showed a prolonged increase in adrenal weight and an attenuated adrenal responsiveness to ACTH in vitro after stressor termination, SDD mice showed reduced dark phase home-cage activity on observation days 7, 14, and 20, flattening of the diurnal corticosterone rhythm, lack of social preference, and higher in vitro IFNγ secretion from mesenteric lymph node cells on day 20/21. Furthermore, the colitis-aggravating effect of SD was more pronounced in SDD than SDL mice following dextran sulfate sodium treatment. In conclusion, the present findings demonstrate that repeated SD effects on behavior, physiology, and immunology strongly depend on the time of day of stressor exposure. Whereas physiological parameters were more affected by SD during the light/inactive phase of mice, behavioral and immunological parameters were more affected by SD during the dark phase. Our results imply that repeated daily SD exposure has a more negative outcome when applied during the dark/active phase. By contrast, the minor physiological changes seen in SDL mice might represent beneficial adaptations preventing the formation of those maladaptive consequences.

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Research works printed but not linked: 47

  1. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G & Schibler U 2000 Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289 2344-2347. (doi:10.1126/science.289.5488.2344) · DOI · Paper page
  2. Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R & Parmigiani S 2005 Social factors and individual vulnerability to chronic stress exposure. Neuroscience & Biobehavioral Reviews 29 67-81. (doi:10.1016/j.neubiorev.2004.06.009) · DOI
  3. Berton O, Aguerre S, Sarrieau A, Mormede P & Chaouloff F 1998 Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats. Neuroscience 82 147-159. (doi:10.1016/S0306-4522(97)00282-0) · DOI
  4. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M et al. 2006 Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 864-868. (doi:10.1126/science.1120972) · DOI · Paper page
  5. de Bodinat C, Guardiola-Lemaitre B, Mocaer E, Renard P, Munoz C & Millan MJ 2010 Agomelatine, the first melatonergic antidepressant: discovery, characterization and development. Nature Reviews. Drug Discovery 9 628-642. (doi:10.1038/nrd3274) · DOI
  6. Deuschle M, Schweiger U, Weber B, Gotthardt U, Korner A, Schmider J, Standhardt H, Lammers CH & Heuser I 1997 Diurnal activity and pulsatility of the hypothalamus-pituitary-adrenal system in male depressed patients and healthy controls. Journal of Clinical Endocrinology and Metabolism 82 234-238. (doi:10.1210/jc.82.1.234) · DOI · Paper page
  7. Gorka Z, Moryl E & Papp M 1996 Effect of chronic mild stress on circadian rhythms in the locomotor activity in rats. Pharmacology, Biochemistry and Behavior 54 229-234. (doi:10.1016/0091-3057(95)02173-6) · DOI
  8. Grippo AJ, Beltz TG & Johnson AK 2003 Behavioral and cardiovascular changes in the chronic mild stress model of depression. Physiology & Behavior 78 703-710. (doi:10.1016/S0031-9384(03)00050-7) · DOI
  9. Herbert J 1997 Fortnighly review, Stress, the brain, and mental illness. BMJ 315 530-535. (doi:10.1136/bmj.315.7107.530) · DOI
  10. Hirschfeld RM 2000 History and evolution of the monoamine hypothesis of depression. Journal of Clinical Psychiatry 61 (Suppl 6) 4-6.
  11. Jiang WG, Li SX, Zhou SJ, Sun Y, Shi J & Lu L 2011 Chronic unpredictable stress induces a reversible change of PER2 rhythm in the suprachiasmatic nucleus. Brain Research 1399 25-32. (doi:10.1016/j.brainres.2011.05.001) · DOI
  12. Kant GJ, Mougey EH & Meyerhoff JL 1986 Diurnal variation in neuroendocrine response to stress in rats: plasma ACTH, b-endorphin, b-LPH, corticosterone, prolactin and pituitary cyclic AMP responses. Neuroendocrinology 43 383-390. (doi:10.1159/000124553) · DOI
  13. Katz MM, Bowden CL & Frazer A 2010 Rethinking depression and the actions of antidepressants: uncovering the links between the neural and behavioral elements. Journal of Affective Disorders 120 16-23. (doi:10.1016/j. jad.2009.08.011) · DOI
  14. Konturek PC, Brzozowski T & Konturek SJ 2011 Gut clock: implication of circadian rhythms in the gastrointestinal tract. Journal of Physiology and Pharmacology 62 139-150.
  15. Lagace DC, Donovan MH, DeCarolis NA, Farnbauch LA, Malhotra S, Berton O, Nestler EJ, Krishnan V & Eisch AJ 2010 Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. PNAS 107 4436-4441. (doi:10.1073/pnas.0910072107) · DOI · Paper page
  16. Levenstein S, Prantera C, Varvo V, Scribano ML, Andreoli A, Luzi C, Arca M, Berto E, Milite G & Marcheggiano A 2000 Stress and exacerbation in ulcerative colitis: a prospective study of patients enrolled in remission. American Journal of Gastroenterology 95 1213-1220. (doi:10.1111/j.1572- 0241.2000.02012.x · DOI · Paper page
  17. Liebsch G, Montkowski A, Holsboer F & Landgraf R 1998 Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety- related behaviour. Behavioural Brain Research 94 301-310. (doi:10.1016/ S0166-4328(97)00198-8) · DOI
  18. Moreau JL, Scherschlicht R, Jenck F & Martin JR 1995 Chronic mild stress- induced anhedonia model of depression; sleep abnormalities and curative effects of electroshock treatment. Behavioural Pharmacology 6 682-687. (doi:10.1097/00008877-199511000-00003) · DOI
  19. Nader N, Chrousos GP & Kino T 2010 Interactions of the circadian CLOCK system and the HPA axis. Trends in Endocrinology and Metabolism 21 277-286. (doi:10.1016/j.tem.2009.12.011) · DOI · Paper page
  20. Obermeier F, Dunger N, Strauch UG, Grunwald N, Herfarth H, Scholmerich J & Falk W 2003 Contrasting activity of cytosin-guanosin dinucleotide oligonucleotides in mice with experimental colitis. Clinical and Experimental Immunology 134 217-224. (doi:10.1046/j.1365-2249.2003.02288.x · DOI
  21. Ottenweller JE, Servatius RJ & Natelson BH 1994 Repeated stress persistently elevates morning, but not evening, plasma corticosterone levels in male rats. Physiology & Behavior 55 337-340. (doi:10.1016/0031-9384(94)90143-0) · DOI
  22. Perez-Cruz C, Simon M, Flugge G, Fuchs E & Czeh B 2009 Diurnal rhythm and stress regulate dendritic architecture and spine density of pyramidal neurons in the rat infralimbic cortex. Behavioural Brain Research 205 406-413. (doi:10.1016/j.bbr.2009.07.021) · DOI
  23. Racagni G, Riva MA & Popoli M 2007 The interaction between the internal clock and antidepressant efficacy. International Clinical Psychopharmacology 22 (Suppl 2) S9-S14. (doi:10.1097/01.yic.0000277957.75852. · DOI
  24. Razzoli M, Carboni L, Andreoli M, Ballottari A & Arban R 2011 Different susceptibility to social defeat stress of BalbC and C57BL6/J mice. Behavioural Brain Research 216 100-108. (doi:10.1016/j.bbr.2010.07.014) · DOI · Paper page
  25. Reber SO 2011 Stress and animal models of inflammatory bowel disease -an update on the role of the hypothalamo-pituitary-adrenal axis. Psychoneuroendocrinology 37 1-19. (doi:10.1016/j.psyneuen.2011.05.014) · DOI
  26. Reber SO, Obermeier F, Straub RH, Falk W & Neumann ID 2006 Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology 147 4968-4976. (doi:10.1210/en.2006-0347) · DOI
  27. Reber SO, Birkeneder L, Veenema AH, Obermeier F, Falk W, Straub RH & Neumann ID 2007 Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 148 670-682. (doi:10.1210/en.2006-0983) · DOI
  28. Reber SO, Obermeier F, Straub RH, Veenema AH & Neumann ID 2008 Aggravation of DSS-induced colitis after chronic subordinate colony (CSC) housing is partially mediated by adrenal mechanisms. Stress 11 225-234. (doi:10.1080/10253890701733351) · DOI
  29. Rybkin II, Zhou Y, Volaufova J, Smagin GN, Ryan DH & Harris RB 1997 Effect of restraint stress on food intake and body weight is determined by time of day. American Journal of Physiology 273 R1612-R1622.
  30. Sachser N & Lick C 1989 Social stress in guinea pigs. Physiology & Behavior 46 137-144. (doi:10.1016/0031-9384(89)90246-1) · DOI
  31. Sanchez MM, Aguado F, Sanchez-Toscano F & Saphier D 1998 Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139 579-587. (doi:10.1210/en. 139.2.579) · DOI
  32. Savignac HM, Hyland NP, Dinan TG & Cryan JF 2011 The effects of repeated social interaction stress on behavioural and physiological parameters in a stress-sensitive mouse strain. Behavioural Brain Research 216 576-584. (doi:10.1016/j.bbr.2010.08.049) · DOI
  33. Sgoifo A, Pozzato C, Meerlo P, Costoli T, Manghi M, Stilli D, Olivetti G & Musso E 2002 Intermittent exposure to social defeat and open-field test in rats: acute and long-term effects on ECG, body temperature and physical activity. Stress 5 23-35. (doi:10.1080/102538902900012387) · DOI
  34. Shalev AY 2009 Posttraumatic stress disorder and stress-related disorders. Psychiatric Clinics of North America 32 687-704. (doi:10.1016/j.psc. 2009.06.001) · DOI
  35. Singewald GM, Nguyen NK, Neumann ID, Singewald N & Reber SO 2009 Effect of chronic psychosocial stress-induced by subordinate colony (CSC) housing on brain neuronal activity patterns in mice. Stress 12 58-69. (doi:10.1080/10253890802042082) · DOI
  36. Slattery DA, Hudson AL & Nutt DJ 2004 Invited review: the evolution of antidepressant mechanisms. Fundamental & Clinical Pharmacology 18 1-21. (doi:10.1111/j.1472-8206.2004.00195.x · DOI
  37. Slattery DA, Uschold N, Magoni M, Bar J, Popoli M, Neumann ID & Reber SO 2011 Behavioural consequences of two chronic psychosocial stress paradigms: anxiety without depression. Psychoneuroendocrinology 37 702-714. (doi:10.1016/j.psyneuen.2011.09.002) · DOI
  38. Tornatzky W & Miczek KA 1993 Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiology & Behavior 53 983-993. (doi:10.1016/0031-9384(93)90278-N) · DOI · Paper page
  39. Uschold-Schmidt N, Nyuyki KD, Fuchsl AM, Neumann ID & Reber SO 2012 Chronic psychosocial stress results in sensitization of the HPA axis to acute heterotypic stressors despite a reduction of adrenal in vitro ACTH responsiveness. Psychoneuroendocrinology 37 1676-1687. (doi:10.1016/j. psyneuen.2012.02.015) · DOI
  40. Ushijima K, Morikawa T, To H, Higuchi S & Ohdo S 2006 Chronobiological disturbances with hyperthermia and hypercortisolism induced by chronic mild stress in rats. Behavioural Brain Research 173 326-330. (doi:10.1016/ j.bbr.2006.06.038) · DOI
  41. Willner P 1990 Animal models of depression: an overview. Pharmacology & Therapeutics 45 425-455. (doi:10.1016/0163-7258(90)90076-E) · DOI
  42. Winkler D, Pjrek E, Praschak-Rieder N, Willeit M, Pezawas L, Konstantinidis A, Stastny J & Kasper S 2005 Actigraphy in patients with seasonal affective disorder and healthy control subjects treated with light therapy. Biological Psychiatry 58 331-336. (doi:10.1016/j. biopsych.2005.01.031) · DOI
  43. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M & Tei H 2000 Resetting central and peripheral circadian oscillators in transgenic rats. Science 288 682-685. (doi:10.1126/science.288.5466.682) · DOI · Paper page
  44. Yamazaki S, Yoshikawa T, Biscoe EW, Numano R, Gallaspy LM, Soulsby S, Papadimas E, Pezuk P, Doyle SE, Tei H et al. 2009 Ontogeny of circadian organization in the rat. Journal of Biological Rhythms 24 55-63. (doi:10.1177/ 0748730408328438) · DOI
  45. Yous S, Andrieux J, Howell HE, Morgan PJ, Renard P, Pfeiffer B, Lesieur D & Guardiola-Lemaitre B 1992 Novel naphthalenic ligands with high affinity for the melatonin receptor. Journal of Medicinal Chemistry 35 1484-1486. (doi:10.1021/jm00086a018) · DOI
  46. Zelena D, Mergl Z, Foldes A, Kovacs KJ, Toth Z & Makara GB 2003 Role of hypothalamic inputs in maintaining pituitary-adrenal responsiveness in repeated restraint. American Journal of Physiology. Endocrinology and Metabolism 285 E1110-E1117.
  47. Zohar J & Westenberg HG 2000 Anxiety disorders: a review of tricyclic antidepressants and selective serotonin reuptake inhibitors. Acta Psychiatrica Scandinavica 403 39-49. (doi:10.1111/j.1600-0447.2000.tb10947.x) · DOI

Cited by

Sorted by citations

Authors
Bartlang, M. S., Neumann, I. D., Slattery, D. A., Uschold-Schmidt, N., Kraus, D., Helfrich-Förster, C., & Reber, S. O.
Affiliations
University of Würzburg (DE)
Venue
Journal of Endocrinology
Published
2012-09-20
Volume
215
Issue
3
Pages
425-437
ISSN
  • 0022-0795 (ISSN-L)
  • 1479-6805
OpenAlex
W2102096288
Cited by
49
References
3
Citations by year
2025: 3 · 2024: 2 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 4 · 2017: 6 · 2016: 6 · 2015: 6 · 2014: 9 · 2013: 3
FWCI
2.36
Type
journal article
Language
en
Open access
Locations
  • Journal of Endocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • University of Regensburg Publication Server (University of Regensburg) (acceptedVersion)
Funders
Deutsche Forschungsgemeinschaft
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
  • Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
Keywords
social defeat stress, circadian timing, home cage activity, social preferences, interferon-gamma, mesenteric lymph nodes, colitis, dextran sulfate, stress adaptation, C57BL/6 mice
MeSH terms
Adrenal Glands, Adrenocorticotropic Hormone, Animals, Male, Mice, Inbred C57BL, Stress, Psychological, Dextran Sulfate, Mice

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