Mice selected for extremes in stress reactivity reveal key endophenotypes of major depression: A translational approach

Psychoneuroendocrinology

Volumn 49, Issue 1, 2014, Pages 229-243

  Heinzmann, Jan Michael ^a   Kloiber, Stefan ^a   Ebling Mattos, Gabriele ^a   Bielohuby, Maximilian ^b   Schmidt, Mathias V ^a   Palme, Rupert ^c   Holsboer, Florian ^a   Uhr, Manfred ^a   Ising, Marcus ^a   Touma, Chadi ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Atypical depression; Dex CRH test; HPA axis; Melancholic depression; Mouse model; Stress reactivity

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; BENZODIAZEPINE DERIVATIVE; CORTICOSTERONE; HYDROCORTISONE; MIRTAZAPINE; MOOD STABILIZER; SEROTONIN UPTAKE INHIBITOR; TRICYCLIC ANTIDEPRESSANT AGENT; VENLAFAXINE; ALDOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; DEXAMETHASONE;

ADD ON THERAPY; ADRENAL GLAND; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; CORTICOSTERONE RELEASE; ENDOPHENOTYPE; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HORMONE RESPONSE; HUMAN; HYPOPHYSIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VIVO STUDY; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PREFRONTAL CORTEX; STRESS; ANIMAL; BLOOD; BRAIN; DIAGNOSTIC USE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INBRED MOUSE STRAIN; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TRANSLATIONAL RESEARCH;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ALDOSTERONE; ANIMALS; BRAIN; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DEPRESSIVE DISORDER, MAJOR; DEXAMETHASONE; DISEASE MODELS, ANIMAL; ENDOPHENOTYPES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MICE; MICE, INBRED STRAINS; MIDDLE AGED; PITUITARY GLAND; PITUITARY-ADRENAL SYSTEM; STRESS, PSYCHOLOGICAL; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84922464660     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.07.008     Document Type: Article

References (51)

1. Angst J., Gamma A., Sellaro R., Zhang H., Merikangas K. Toward validation of atypical depression in the community: results of the Zurich cohort study. J. Affect. Disord. 2002, 72:125-138.
2. Antonijevic I.A. Depressive disorders - is it time to endorse different pathophysiologies?. Psychoneuroendocrinology 2006, 31:1-15.
3. Axelrod J., Reisine T.D. Stress hormones: their interaction and regulation. Science 1984, 224:452-459.
4. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 2004, 44:525-557.
5. Dallman M.F., Makara G.B., Roberts J.L., Levin N., Blum M. Corticotrope response to removal of releasing factors and corticosteroids in vivo. Endocrinology 1985, 117:2190-2197.
6. de Kloet E.R., Joels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
7. DeBold C.R., Sheldon W.R., DeCherney G.S., Jackson R.V., Alexander A.N., Vale W., Rivier J., Orth D.N. Arginine vasopressin potentiates adrenocorticotropin release induced by ovine corticotropin-releasing factor. J. Clin. Invest. 1984, 73:533-538.
8. Fenzl T., Touma C., Romanowski C.P., Ruschel J., Holsboer F., Landgraf R., Kimura M., Yassouridis A. Sleep disturbances in highly stress reactive mice: modeling endophenotypes of major depression. BMC Neurosci. 2011, 12:29.
9. Fries E., Hesse J., Hellhammer J., Hellhammer D.H. A new view on hypocortisolism. Psychoneuroendocrinology 2005, 30:1010-1016.
10. Gold P.W., Chrousos G.P. Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol. Psychiatry 2002, 7:254-275.
11. Heinzmann J.M., Thoeringer C.K., Knapman A., Palme R., Holsboer F., Uhr M., Landgraf R., Touma C. Intrahippocampal corticosterone response in mice selectively bred for extremes in stress reactivity: a microdialysis study. J. Neuroendocrinol. 2010, 22:1187-1197.
12. Helmreich D.L., Cullinan W.E., Watson S.J. The effect of adrenalectomy on stress-induced c-fos mRNA expression in the rat brain. Brain Res. 1996, 706:137-144.
13. Henkel V., Mergl R., Allgaier A.K., Kohnen R., Moller H.J., Hegerl U. Treatment of depression with atypical features: a meta-analytic approach. Psychiatry Res. 2006, 141:89-101.
14. Heuser I., Bissette G., Dettling M., Schweiger U., Gotthardt U., Schmider J., Lammers C.H., Nemeroff C.B., Holsboer F. Cerebrospinal fluid concentrations of corticotropin-releasing hormone, vasopressin, and somatostatin in depressed patients and healthy controls: response to amitriptyline treatment. Depress. Anxiety 1998, 8:71-79.
15. Heuser I., Yassouridis A., Holsboer F. The combined dexamethasone/CRH test: a refined laboratory test for psychiatric disorders. J. Psychiatr. Res. 1994, 28:341-356.
16. Hinkelmann K., Moritz S., Botzenhardt J., Riedesel K., Wiedemann K., Kellner M., Otte C. Cognitive impairment in major depression: association with salivary cortisol. Biol. Psychiatry 2009, 66:879-885.
17. Holsboer F., Ising M. Stress hormone regulation: biological role and translation into therapy. Annu. Rev. Psychol. 2010, 61:81-109. C101-C111.
18. Holsboer F., Lauer C.J., Schreiber W., Krieg J.C. Altered hypothalamic-pituitary-adrenocortical regulation in healthy subjects at high familial risk for affective disorders. Neuroendocrinology 1995, 62:340-347.
19. Hunt P.J., Gurnell E.M., Huppert F.A., Richards C., Prevost A.T., Wass J.A., Herbert J., Chatterjee V.K. Improvement in mood and fatigue after dehydroepiandrosterone replacement in Addison's disease in a randomized, double blind trial. J. Clin. Endocrinol. Metab. 2000, 85:4650-4656.
20. Ising M., Weyers P., Janke W., Erdmann G. Test criteria of SVF78 by Janke und Erdmann, a short form of SVF120. Zeitschrift für Differentielle und Diagnostische Psychologie 2001, 22:279-289.
21. Ising M., Horstmann S., Kloiber S., Lucae S., Binder E.B., Kern N., Kunzel H.E., Pfennig A., Uhr M., Holsboer F. Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depression - a potential biomarker?. Biol. Psychiatry 2007, 62:47-54.
22. Karalis K.P., Venihaki M., Zhao J., van Vlerken L.E., Chandras C. NF-kappaB participates in the corticotropin-releasing, hormone-induced regulation of the pituitary proopiomelanocortin gene. J. Biol. Chem. 2004, 279:10837-10840.
23. Kloiber S., Ising M., Reppermund S., Horstmann S., Dose T., Majer M., Zihl J., Pfister H., Unschuld P.G., Holsboer F., Lucae S. Overweight and obesity affect treatment response in major depression. Biol. Psychiatry 2007, 62:321-326.
24. Knapman A., Heinzmann J.M., Hellweg R., Holsboer F., Landgraf R., Touma C. Increased stress reactivity is associated with cognitive deficits and decreased hippocampal brain-derived neurotrophic factor in a mouse model of affective disorders. J. Psychiatr. Res. 2010, 44:566-575.
25. Knapman A., Heinzmann J.M., Holsboer F., Landgraf R., Touma C. Modeling psychotic and cognitive symptoms of affective disorders: disrupted latent inhibition and reversal learning deficits in highly stress reactive mice. Neurobiol. Learn. Mem. 2010, 94:145-152.
26. Knapman A., Kaltwasser S.F., Martins-de-Souza D., Holsboer F., Landgraf R., Turck C.W., Czisch M., Touma C. Increased stress reactivity is associated with reduced hippocampal activity and neuronal integrity along with changes in energy metabolism. Eur. J. Neurosci. 2012, 35:412-422.
27. Lamers F., Vogelzangs N., Merikangas K.R., de Jonge P., Beekman A.T., Penninx B.W. Evidence for a differential role of HPA-axis function, inflammation and metabolic syndrome in melancholic versus atypical depression. Mol. Psychiatry 2013, 18:692-699.
28. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
29. Mattos G.E., Heinzmann J.M., Norkowski S., Helbling J.C., Minni A.M., Moisan M.P., Touma C. CBG contributes to the neuroendocrine phenotype of mice selected for extremes in stress reactivity. J. Endocrinol. 2013, 219:217-229.
30. Metherell L.A., Chapple J.P., Cooray S., David A., Becker C., Ruschendorf F., Naville D., Begeot M., Khoo B., Nurnberg P., Huebner A., Cheetham M.E., Clark A.J. Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nat. Genet. 2005, 37:166-170.
31. Modell S., Lauer C.J., Schreiber W., Huber J., Krieg J.C., Holsboer F. Hormonal response pattern in the combined DEX-CRH test is stable over time in subjects at high familial risk for affective disorders. Neuropsychopharmacology 1998, 18:253-262.
32. Nemeroff C.B., Widerlov E., Bissette G., Walleus H., Karlsson I., Eklund K., Kilts C.D., Loosen P.T., Vale W. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 1984, 226:1342-1344.
33. Raison C.L., Miller A.H. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am. J. Psychiatry 2003, 160:1554-1565.
34. Rydmark I., Wahlberg K., Ghatan P.H., Modell S., Nygren A., Ingvar M., Asberg M., Heilig M. Neuroendocrine, cognitive and structural imaging characteristics of women on longterm sickleave with job stress-induced depression. Biol. Psychiatry 2006, 60:867-873.
35. Sonino N., Fava G.A., Raffi A.R., Boscaro M., Fallo F. Clinical correlates of major depression in Cushing's disease. Psychopathology 1998, 31:302-306.
36. Starkman M.N., Schteingart D.E., Schork M.A. Cushing's syndrome after treatment: changes in cortisol and ACTH levels, and amelioration of the depressive syndrome. Psychiatry Res. 1986, 19:177-188.
37. Stetler C., Miller G.E. Depression and hypothalamic-pituitary-adrenal activation: a quantitative summary of four decades of research. Psychosom. Med. 2011, 73:114-126.
38. Thomsen A.F., Kvist T.K., Andersen P.K., Kessing L.V. The risk of affective disorders in patients with adrenocortical insufficiency. Psychoneuroendocrinology 2006, 31:614-622.
39. Thomson F., Craighead M. Innovative approaches for the treatment of depression: targeting the HPA axis. Neurochem. Res. 2008, 33:691-707.
40. Touma C., Bunck M., Glasl L., Nussbaumer M., Palme R., Stein H., Wolferstatter M., Zeh R., Zimbelmann M., Holsboer F., Landgraf R. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 2008, 33:839-862.
41. Touma C., Fenzl T., Ruschel J., Palme R., Holsboer F., Kimura M., Landgraf R. Rhythmicity in mice selected for extremes in stress reactivity: behavioural, endocrine and sleep changes resembling endophenotypes of major depression. PLoS ONE 2009, 4:e4325.
42. Touma C., Gassen N.C., Herrmann L., Cheung-Flynn J., Bull D.R., Ionescu I.A., Heinzmann J.M., Knapman A., Siebertz A., Depping A.M., Hartmann J., Hausch F., Schmidt M.V., Holsboer F., Ising M., Cox M.B., Schmidt U., Rein T. FK506 binding protein 5 shapes stress responsiveness: modulation of neuroendocrine reactivity and coping behavior. Biol. Psychiatry 2011, 70:928-936.
43. Touma C., Palme R., Sachser N. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm. Behav. 2004, 45:10-22.
44. Touma C., Sachser N., Mostl E., Palme R. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 2003, 130:267-278.
45. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009, 10:397-409.
46. Wahlberg K., Ghatan P.H., Modell S., Nygren A., Ingvar M., Asberg M., Heilig M. Suppressed neuroendocrine stress response in depressed women on job-stress-related long-term sick leave: a stable marker potentially suggestive of preexisting vulnerability. Biol. Psychiatry 2009, 65:742-747.
47. Walker E.F., Trotman H.D., Pearce B.D., Addington J., Cadenhead K.S., Cornblatt B.A., Heinssen R., Mathalon D.H., Perkins D.O., Seidman L.J., Tsuang M.T., Cannon T.D., McGlashan T.H., Woods S.W. Cortisol levels and risk for psychosis: initial findings from the North American prodrome longitudinal study. Biol. Psychiatry 2013, 74:410-417.
48. Wang S.S., Kamphuis W., Huitinga I., Zhou J.N., Swaab D.F. Gene expression analysis in the human hypothalamus in depression by laser microdissection and real-time PCR: the presence of multiple receptor imbalances. Mol. Psychiatry 2008, 13(786-799):741.
49. Wardenaar K.J., Vreeburg S.A., van Veen T., Giltay E.J., Veen G., Penninx B.W., Zitman F.G. Dimensions of depression and anxiety and the hypothalamo-pituitary-adrenal axis. Biol. Psychiatry 2011, 69:366-373.
50. Weiser M.J., Osterlund C., Spencer R.L. Inhibitory effects of corticosterone in the hypothalamic paraventricular nucleus (PVN) on stress-induced adrenocorticotrophic hormone secretion and gene expression in the PVN and anterior pituitary. J. Neuroendocrinol. 2011, 23:1231-1240.
51. Zobel A.W., Nickel T., Sonntag A., Uhr M., Holsboer F., Ising M. Cortisol response in the combined dexamethasone/CRH test as predictor of relapse in patients with remitted depression. a prospective study. J. Psychiatr. Res. 2001, 35:83-94.