Effects of chronic mild stress (CMS) and imipramine administration, on spleen mononuclear cell proliferative response, serum corticosterone level and brain norepinephrine content in male mice

Psychoneuroendocrinology

Volumn 24, Issue 3, 1999, Pages 345-361

  Azpiroz, A ^a   Fano, E ^a   Garmendia, L ^a   Arregi, A ^a   Cacho, R ^a   Beitia, G ^a   Brain, P F ^b  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Chronic mild stress; Corticosterone; Imipramine; Immunoreactivity; Mice; Norepinephrine

Indexed keywords

CORTICOSTERONE; IMIPRAMINE; NORADRENALIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; DEPRESSION; DOSE TIME EFFECT RELATION; DRUG EFFICACY; DRUG MECHANISM; EMOTIONAL STRESS; FLUID INTAKE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; NORADRENALIN BRAIN LEVEL; NORADRENALIN RELEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PSYCHOPHARMACOTHERAPY; SYMPATHETIC FUNCTION; TRANQUILIZING ACTIVITY;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; BRAIN; CELL DIVISION; CHRONIC DISEASE; CORTICOSTERONE; DIETARY SUCROSE; HIPPOCAMPUS; HYPOTHALAMUS; IMIPRAMINE; MALE; MICE; NOREPINEPHRINE; SPLEEN; STRESS;

EID: 0033022164     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4530(98)00084-5     Document Type: Article

References (94)

1. Adell A., García-Marquez C., Armario A., Gelpi E. Effects of chronic stress on serotonin and noradrenaline in the rat brain. Biogenic Amines. 7:1990;19-26.
2. Asterita M.F. The Physiology of Stress. 1985;Human Sciences Press, New York.
3. Audus K.L., Gordon M.A. Tricyclic antidepressant effects on the murine lymphocyte mitogen response. J. Immunopathol. 4:1982;13-27.
4. Ayensu W.K., Pucilowski O., Mason G.A., Overstreet D.H., Rezvani A.H., Janowski D.S. Effects of chronic mild stress on serum complement activity, saccharin preference, and corticosterone levels in flinders lines of rats. Physiol. Behav. 57:1995;165-169.
5. Baldessarini R.J. The basis for amine hypotheses in affective disorder: a critical evaluation. Arch. Gen. Psychiatry. 32:1975;1087-1093.
6. Bateman A., Singh A., Kral T., Solomon S. The immune hypothalamic-pituitary-adrenal axis. Endocr. Rev. 10:1989;92-112.
7. Besedovsky H., del Rey A.E., Sorkin E., da Prada M., Keller H.H. Immunoregulation mediated by the sympathetic nervous system. Cell. Immunol. 48:1979;346-355.
8. Blalock E.J. Neuroimmunoendocrinology. 1993;Karger, Basle.
9. Brain P.F., Marrow L.P. Rodent 'models' of human neuroses and psychoses. Haug M., Whalen R.E Brain Behavior and Cognition. 1998;APA, Washington.
10. Brown G.W., Harris T. Life Events and Illness. 1988;Guilford Press, New York.
11. Calabrese J.R., Kling M.A., Gold P.W. Alterations in immunocompetence during stress, bereavement, and depression: focus on neuroendocrine regulation. Am. J. Psychiatry. 144:1987;1123-1134.
12. Cannon W.B., de la Paz D. Emotional stimulation of adrenal secretion. Am. J. Psychiatry. 28:1991;64-70.
13. Chikanza Y.C., Grossman A.B. Neuroendocrine immune responses to inflammation: the concept of the neuroendocrine immune loop. Baillieres Clin. Reumathol. 10:1996;199-225.
14. Dantzer R., Kelley K.W. Stress and immunity: an integrated view of the relationships between the brain and the immune system. Life Sci. 44:1989;1995-2008.
15. Dantzer R., Bluthe R.M., Kent S., Goodall G. Behavioral effects of cytokines: an insight into mechanisms of sickness behavior. Methods Neurosci. 17:1993;130-150.
16. Devoino L., Morozova N., Cheido M. Participation of serotoninergic system in neuroimmunomodulation: intraimmune mechanisms and the pathways providing an inhibitory effect. Int. J. Neurosci. 40:1988;111-128.
17. Dunn A.J. Systemic interleukin-1 administration stimulates hypothalamic norepinephrine metabolism paralleling the increased plasma corticosterone. Life Sci. 43:1988;429-435.
18. Dunn A.J., Powell M.L., Meitin C., Small P.A. Jr. Virus infection as a stressor: influenza virus elevates plasma concentrations of corticosterone, and brain concentrations of MHPG and tryptophan. Physiol. Behav. 45:1989;591-594.
19. Dunn A.J., Welch J. Stress and endotoxin-induced increases in brain tryptophan and serotonin metabolism depend on sympathetic nervous system activity. J. Neurochem. 57:1991;1615-1622.
20. Dunn A.J. Infection as a stressor: a cytokine-mediated activation of the hypotalamo-pituitary-adrenal axis? Ciba Found. Symp. 172:1993;226-242.
21. Eisen J.N., Irwin J., Quay J., Livnat S. The effect of antidepressants on immune function in mice. Biolog. Psychiatry. 26:1989;805-817.
22. Fawcett J., Clark D.C., Scheftner W.A., Gibbons R.D. Assessing anhedonia in psychiatric patients: the pleasure scale. Arch. Gen. Psychiatry. 40:1983;79-84.
23. Felten D.L., Overhage J.M., Felten S.Y., Schmedtje J.F. Noradrenergic sympathetic innervation of lymphoid tissue in the rabbit appendix. Further evidence for a link between the nervous and immune systems. Brain Res. Bull. 7:1981;595-612.
24. Felten D.L., Livnat S., Felten S.Y., Carlson S.L., Bellinger D.L., Yeh P. Sympathetic innervation of lymph nodes in mice. Brain Res. Bull. 13:1984;693-699.
25. Felten S.Y., Felten D.L., Bellinger D.L., Carlson S.L., Ackerman K.D. Noradrenergic sympathetic innervation of lymphoid organs. Prog. Allergy. 43:1988;14-36.
26. Flores C.M., Hernandez M.C., Hargreaves K.M., Bayer B.M. Restraint stress-induced elevations in plasma corticosterone and β-endorphin are not accompanied by alterations in immune function. J. Neuroimmunol. 28:1990;219-225.
27. Frankenhauser M. The sympathetic-adrenal and pituitary-adrenal response to challenge: Comparison between the sexes. Dembroski T.M., Schmidt T.H., Blunchen G. Biobehavioral Bases of Coronary Heart Disease. 1983;91-105 Karger, New York.
28. Frederickson R.C.A., Hendrie H.C., Hingtgen J.N., Aprison M.H. Neuroregulation of Autonomic, Endocrine and Immune Systems. 1986;Martinus Nijhoff, Boston, MA.
29. Frommberger U.H., Bauer J., Haselbauer P., Fraulin A., Riemann D., Berger M. Interkeukin-6 (IL-6) plasma levels in depression and schizophrenia: comparison between the acute state and after remission. Eur. Arch. Psychiatry Clin. Neurosci. 47:1997;228-233.
30. Guillemin R., Cohn M., Melnechuck T. Neural Modulation of Immunity. 1985;Raven Press, New York.
31. Henry J.P., Stephens P.M. Stress, Health and the Social Environment. 1977;Springer, New York.
32. Herber T.B., Cohen S. Depression and immunity: a meta-analytic review. Psycholog. Bull. 113:1993;472-486.
33. Hilakivi-Clarke L.A., Arora P.K., Sabol M.B., Clarke R., Dickson R.B., Lippman M.E. Alterations in behavior, steroid hormones and natural killer cell activity in male transgenic TGFα mice. Brain Res. 588:1992;97-103.
34. Hoffman-Goetz L., Thorne R.J., Houston M.E. Splenic immune responses following treadmill exercise in mice. Can. J. Physiol. Pharmacol. 66:1988;1405-1419.
35. Irwin M., Caldwell C., Smith T.L., Brown S., Schuckit N.A., Gillin J.C. Major depressive disorder, alcoholism, and reduced natural killer cell cytotoxicity. Arch. Gen. Psychiatry. 47:1990;713-718.
36. Jahnova E. The role of serotonin in the regulation of the immune response. Bratisl. Lek. Listy. 95:1994;181-184.
37. Jessop J.J., Gale K., Bayer B.M. Enhancement of rat lymphocyte proliferation after prolonged exposure to stress. J. Neuroimmunol. 16:1987;261-271.
38. Jessop J.J., Gale K., Bayer B.M. Time-depending enhancement of lymphocyte activation by mitogens after exposure to isolation or water scheduling. Life Sci. 43:1988;1133-1140.
39. Jessop J.J., Bayer B.M. Time-dependent effects of isolation on lymphocyte and adrenocortical activity. J. Neuroimmunol. 23:1989;143-147.
40. Kelley S.M., Livnat S. Catecholamines and immunologic activity. Ader R., Felten D.L., Cohen N. Psychoneuroimmunology. 1991;Academic Press, San Diego, CA.
41. Kiecolt-Glaser J.K., Glaser R. Stress and immune function in humans. Ader R., Felten D.L., Cohen N. Psychoneuroimmunology. 1991;Academic Press, San Diego, CA.
42. Kort W.J., Weijma J.M. Effect of chronic light-dark shift stress on the immune response of the rat. Physiol. Behav. 29:1982;183-187.
43. Kronfol Z., House D.J. Lymphocyte mitogenesis, immunoglobulin and complement levels in depressed patients and normal controls. Acta Psychiatr. Scand. 80:1989;142-147.
44. Kubera M., Basta-Kaim A., Gorka Z. The effect of amitriptyline on the cell-mediated immunity of stressed rats. Pol. J. Pharmacol. Pharm. 47:1995;137-142.
45. Kubera M., Basta-Kaim A., Papp M. The effect of chronic treatment with imipramine on the immunoreactivity of animals subjected to a chronic mild stress model of depression. Immunopharmacology. 30:1995;225-230.
46. Kubera M., Symbirtsev A., Basta-Kaim A., Borycz J., Roman A., Papp M., Claesson M. Effect of chronic treatment with imipramine on interleukin-1 and interleukin-2 production by splenocytes obtained from rats subjected to a chronic mild stress model of depression. Pol. J. Pharmacol. Pharm. 48:1996;503-506.
47. Leibowitz S.F., Diaz S., Tempel D. Norepinephrine in the paraventricular nucleus stimulates corticosterone release. Brain Res. 496:1989;219-227.
48. LeMay L.G., Vander A.J., kluger M.J. The effects of psychological stress on plasma interleukin-6 activity in rats. Physiol. Behav. 47:1990;957-961.
49. Leonard B.E., Song C. Stress and the immune system in the etiology of anxiety and depression. Pharmacol. Biochem. Behav. 54:1996;299-303.
50. Levine S., Ursin H. Coping and Health. 1980;Plenum Press, New York.
51. Linthorst A.C., Flachskamm C., Muller Preuss M., Holsboer F., Reul J.M. Effect of bacterial endotoxin and interleukin-1β on hippocampal serotoninergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J. Neurosci. 15:1995;2920-2934.
52. Livnat S., Felten S.Y., Carlson S.L., Lorton Bellinger D., Felten D.L. Involvement of peripheral and central catecholamine systems in neural immune interactions. J. Neuroimmunol. 10:1985;5-30.
53. Lloyd C. Life events and depressive disorders reviewed. 2. Events as precipitating factors. Arch. Gen. Psychiatry. 32:1980;541-548.
54. Locke S., Ader R., Besedovsky H., Hall N., Solomon G., Strom T. Foundations of Psychoneuroimmunology. 1985;Aldine, New York.
55. Maes M. Evidence for an immune response in major depression: A review and hypothesis. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 19:1995;11-38.
56. Maes M., Plancken V.D., Stevens W.J., Peeters L.S., DeClerk L.S., Bridts C.H., Schotte C., Csyns P. Leukocytosis, monocytosis and neutrophilia: hallmarks of severe depression. J. Psychiatric Res. 26:1992;125-134.
57. Maes M., Stevens W., DeClerk L., Bridts C., Peeters D., Schotte C., Cosyns P. Immune disorders in depression: higher T helper/T suppressor-cytotoxic cell ratio. Acta Psychiatr. Scand. 86:1992;423-431.
58. Maes M., Meltzer H.Y., Bosmans E., Bergmans R., Vandoolaeghe E., Ranjan R., Desnyder R. Increased serum concentrations of interkeukin-6, soluble interleukin-6, soluble interleukin-2 and transferrin receptor in major depression. J. Affect. Disorders. 34:1995;301-309.
59. Maes M., Bosmans E., De-Jongh R., Kenis G., Vandoolaeghe E., Neels H. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine. 9:1997;853-858.
60. Maier S.F., Watkins L.R., Fleshner M. Psychoneuroimmunology. The interface between behavior, brain and immunity. Am. Psychol. 49:1994;1004-1017.
61. Matta S., Singh J., Newton R., Sharp B.M. The adrenocorticotropin response to interleukin-1β instilled into the rat median eminence depends on the local release of catecholamines. Endocrinology. 127:1990;2175-2182.
62. Miller A.H., Spencer R.L., McEwen B.S., Stein M. Depression, adrenal steroids and the immune system. Ann. Med. 25:1993;481-487.
63. Mohankumar P.S., Thyagarajan S., Quadri S.K. Interleukin-1 stimulates the release of dopamine and dihydroxyphenylacetic acid from the hypothalamus in vivo. Life Sci. 48:1991;925-930.
64. Mohl P.C., Huang L., Bowden C., Fischbach M., Vogtsberger K., Talal N. Natural killer cell activity in major depression. Am. J. Psychiatry. 144:1987;16-19.
65. Monjan A.A., Collector M.I. Stress-induced modulation of the immune response. Science. 196:1977;307-308.
66. Monleon S., D'Aquila P., Parra A., Simón V.M., Brain P.F., Wilner P. Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine. Psychopharmacology. 117:1995;453-457.
67. Moreau J.L., Jenck F., Martin J.R., Mortas P., Haecely W.E. Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmental self-stimulation behavior in rats. Eur. Neuropsychopharmacol. 2:1992;43-49.
68. Mormede P., Dantzer R., Michaud B., Kelley K.W., Le Moal M. Influence of stressor predictability and behavioral control on lymphocyte reactivity, antibody responses and neuroendocrine activation in rats. Physiol. Behav. 43:1988;577-583.
69. Muller N., Ackenheil N., Hofschuster E. Altered T-cell number and reduced suppressor cell activity in patients with affective psychosis. Hadden J.W., Masek K., Nistico G. Interactions among Central Nervous System, Neuroendocrine and Immune Systems. 1989;385-394 Pythagora Press, Rome.
70. O'Leary A. Stress, emotion and human immune function. Psychol. Bull. 108:1990;363-382.
71. Papp M., Willner P., Muscat R. An animal model of anhedonia. Attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology. 104:1991;255-259.
72. Papp M., Lappas S., Muscat R., Willner P. Attenuation of place preference conditioning but not place aversion conditioning by chronic mild stress. J. Pshychopharmacol. 6:1992;352-386.
73. Papp M., Klimek V., Willner P. Effects of imipramine on serotonergic and β-adrenergic receptor binding in a realistic animal model of depression. Psychopharmacology. 114:1994;309-314.
74. Plotnikoff N.P., Miller G.C. Enkephalins as immunomodulators. Int. J. Immunopharmacol. 5:1983;437-446.
75. Reid Y., Forbes N., Stewart C., Matthews K. Chronic mild stress and depressive disorder: a useful model? Psychopharmacology. 134:1997;365-367.
76. Sandi C., Cambronero J.C., Borrel J., Guaza C. Effects of HPA hormones on adapted lymphocyte responsiveness to repeated stress. Brain Res. Bull. 28:1992;581-585.
77. Schleifer S.J., Keller S.E., Bond R.N., Cohen J., Stein M. Major depressive disorder and immunity: role of age, sex, severity and hospitalization. Arch. Gen. Psychiatry. 46:1989;81-87.
78. Seidel A., Arolt V., Hunstiger M., Rink L., Behnisch A., Kirchner H. Increased CD56+ natural killer cells and related cytokines in major depression. Clin. Immunol. Immunopathol. 78:1996;83-85.
79. Sluzewska A., Rybakowski J., Bosmann E., Sobieska M., Berghmans R., Maes M., Wiktorowicz K. Indicators of immune activation in major depression. Psychiatry Res. 64:1996;161-167.
80. Selye H. The Stress of Life. 1956;McGraw-Hill, New York.
81. Smagin G.N., Swiergiel A.H., Dunn A.J. Peripheral administration of interleukin-1 increases extracellular concentrations of norepinephrine in rat hypothalamus: comparison with plasma corticosterone. Psychoneuroendocrinology. 21:1996;83-93.
82. Stamford J.A., Muscat R., O'Connor J.J., Patel J., Trout S.J., Wieczorek W.J., Kruk Z.L., Willner P. Voltammetric evidence that subsensitivity to reward following chronic mild stress is associated with increased release of mesolimbic dopamine. Psychopharmacology. 105:1991;275-282.
83. Stein M., Miller A.H., Trestman R.L. Depression, the immune system, and health and illness. Arch. Gen. Psychiatry. 48:1991;171-177.
84. Sternberg E.M. Neuroendocrine factors in susceptibility to inflammatory disease: focus on the hypothalamic-pituitary-adrenal axis. Horm. Res. 43:1995;159-161.
85. Tolis G., Labrie F., Martin J.B., Naftolin F. Clinical Neuroendocrinology: A Pathophysiological Approach. 1979;Raven Press, New York.
86. Vetulani J. The development of our understanding of the mechanism of action of antidepressant drugs. Pol. J. Pharmacol. Pharm. 43:1991;323-338.
87. Wagner J., Palfreyman M.G., Zraika M. Determination of dopa, dopamine, dopac, epinephrine, norepinephrine, alpha-monofluoromethyldopa and alpha-difluoromethyldopa in various tissues of mice and rats using reversed-phase ion-pair liquid chromatography with electrochemical detection. J. Chromatogr. 164:1979;41-54.
88. Weidenfeld J., Abramsky O., Ovadia H. Evidence for the involvement of the central adrenergic system in interleukin-1 induced adrenocortical response. Neuropharmacology. 28:1989;1411-1414.
89. Weisse C.S. Depression and immunocompetence: a review of the literature. Psychol. Bull. 111:1992;475-489.
90. Willner P., Towell A., Sampson D., Muscat R., Sophokleous S. Reduction of sucrose preference by chronic mild stress and its restoration by a tricyclic antidepressant. Psychopharmacology. 93:1987;358-364.
91. Willner P., Golembiowska K., Klimek V., Muscat R. Changes in mesolimbic dopamine may explain stress-induced anhedonia. Psychobiology. 19:1991;79-84.
92. Willner P., Muscat R., Papp M. Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci. Biobehav. Rev. 16:1992;525-534.
93. Xia Z., DePierre J.W., Nassberger L. Tricyclic antidepressants inhibit IL-6, IL-1β and TNF-α release in human blood monocytes and IL-2 and interferon-γ in T-cells. Immunopharmacology. 34:1996;27-37.
94. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 711:1966;163-174.