Negative immunoregulatory effects of antidepressants inhibition of interferon-γ and stimulation of interleukin-10 secretion

Neuropsychopharmacology

Volumn 20, Issue 4, 1999, Pages 370-379

  Maes, Michael ^a,b   Song, Cai ^a   Lin, Ai Hua ^a,c   Bonaccorso, Stefania ^d   Kenis, Gunter ^e   De Jongh, Raf ^e   Bosmans, Eugene ^f   Scharpé, Simon ^c  

^a Clinical Research Center for Mental Health of Antwerp   (Belgium)

^b VANDERBILT UNIVERSITY   (United States)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e AZ Oost Limburg ^*  (Belgium)

^f Eurogenetics   (Belgium)

Author keywords

Antidepressants; Cytokines; Depression; Interferon ; Interleukin 10

Indexed keywords

ANTIDEPRESSANT AGENT; CLOMIPRAMINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PHYTOHEMAGGLUTININ; SERTRALINE; TRAZODONE;

ADULT; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; DEPRESSION; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IN VITRO STUDY; MALE; MONOCYTE; NORMAL HUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ADULT; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; ANTIDEPRESSIVE AGENTS, TRICYCLIC; ANTIVIRAL AGENTS; CLOMIPRAMINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; INTERFERON-GAMMA, RECOMBINANT; INTERLEUKIN-10; MALE; SEROTONIN UPTAKE INHIBITORS; SERTRALINE; TRAZODONE;

EID: 0033057940     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0893-133X(98)00088-8     Document Type: Article

References (78)

1. Angel J.B., Saget B.M., Walsh S.P., Greten T.F., Dinarello C.A., Skolnik P.R., Endres S. Rolipram, a specific type IV phosphodiesterase inhibitor, is a potent inhibitor of HIV-1 replication. Aids. 9:1995;1137-1144.
2. Aune T.M., Golden H.W., McGrath K.M. Inhibitors of serotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo. J Immunol. 153:1994;489-498.
3. Bengtsson B.-O., Zhu J., Thorell L.-H., Olsson T., Link H., Walinder J. Effects of zimeldine and its metabolites, clomipramine, imipramine and maprotiline in experimental allergic neuritis in Lewis rats. J Neuroimmunol. 39:1992;109-122.
4. Bluthé R.M., Crestani F., Kelley K.W., Dantzer R. Mechanisms of the behavior effects of interleukin 1. Ann NY Acad Sci. 650:1992;268-275.
5. Bonaccorso S, Lin A, Verkerk R, Van Hunsel F, Libbrecht I, Scharpé S, DeClerck L, Biondi M, Janca A, Maes M (1998): Immune markers in fibromyalgia: Comparison with major depressed patients and normal volunteers. J Affect Disord 48:75-82.
6. Bondesson L., Nordlind K., Liden S., Sundstrom E. Inhibiting effects of serotonin and serotonin antagonists on the migration of mononuclear leucocytes. Immunopharmacol Immunotoxicol. 15:1993;243-250.
7. Bonnet M., Lespinats G., Burtin C. Histamine and serotonin suppression of lymphocyte response to phytohemagglutinin and antigen. Cell Immunol. 83:1984;280-291.
8. Calabrese J.R., Skwerer R.G., Barana B., Gulledge A.D., Valenzuela R., Butkus A., Subichin S., Krupp N.E. Depression, immunocompetence, and prostaglandins of the E series. Psychiatr Res. 17:1986;41-47.
9. Cavaillon J-M (1996): Interleukin-6, in Les Cytokines, Cavaillon J-M, ed., Paris, Masson, pp. 184-199.
10. Dayer J.-M., Burger D. Interleukin-1, tumor necrosis factor and their specific inhibitors. Eur Cytokine Netw. 5:1994;563-571.
11. De Groote D., Zangerle P.F., Gevaert Y., Fassotte M.F., Beguin Y., Noizat-Pirenne F., Pirenne J., Gathy R., Lopez M., Dehart I., Igot D., Baudrihaye M., Delacroix D., Franchimont P. Direct stimulation of cytokines (IL-1β, TNF-α, IL-6, IL-2, IFN-γ and GM-CSF) in whole blood. I. Comparison with isolated PBMC stimulation. Cytokine. 4:1992;239-248.
12. De Groote D., Gaevaert Y., Lopez M., Gathy R., Fauchet F., Dehart I., Jadoul M., Radoux D., Franchimont P. Novel method for the measurement of cytokine production by one-stage procedure. J Immunol Methods. 9:1993;259-267.
13. Dinarello C.A. The biological properties of interleukin-1. Eur Cytokine Netw. 5:1994;517-531.
14. Duch D.S., Woolf J.H., Nichol C.A., Davidson J.R., Garbutt J.C. Urinary excretion of biopterin and neopterin in psychiatric disorders. Psychiatr Res. 11:1984;83-89.
15. Dunbar P.R., Hill J., Neale T.J., Mellsop G.W. Neopterin measurement provides evidence of altered cell-mediated immunity in patients with depression, but not with schizophrenia. Psychol Med. 22:1992;1051-1057.
16. Eckmann F., Fichte K., Meya U., Sastre-y-Hernandez M. Rolipram in major depression. Results of a double-blind comparative study with amitriptyline Curr Ther Res. 43:1988;291-295.
17. Faraj B.A., Olkowski Z.L., Jackson R.T. Expression of a high-affinity serotonin transporter in human lymphocytes. Int J Immunopharmacol. 16:1994;561-567.
18. Frommberger U.H., Bauer J., Haselbauer P., Fraulin A., Riemann D., Berger M. Interleukin-6 (IL-6) plasma levels in depression and schizophrenia. Comparison between the acute state and after remission Eur Arch Psychiatry Clin Neurosci. 247:1997;228-233.
19. Greten T.F., Eigler A., Sinha B., Moeller J., Endres S. The specific type IV phosphodiesterase inhibitor rolipram differentially regulates the proinflammatory mediators TNF-alpha and nitric oxide. Int J Immunopharmacol. 17:1995;605-610.
20. Gutterman J.U., Fein S., Quesada J., Horning S.J., Levine J.F., Alexanian R., Bernhardt L., Kramer M., Spiegel H., Colburn W., Trown P., Merigan T., Dziewanowski Z. Recombinant leukocyte A interferon. Pharmacokinetics, single dose tolerance, and biologic effects in cancer patients Ann Int Med. 96:1982;549-556.
21. Herbert T.B., Cohen S. Depression and immunity. A meta-analytic review Psychol Bull. 113:1993;472-486.
22. Horowski R., Sastre-y-Hernandez M. Clinical effects of the neurotropic selective cAMP phoshodiesterase inhibitor rolipram in depressed patients. Global evaluation of the preliminary reports Curr Ther Res. 38:1985;23-29.
23. Idova G.V., Cheido M.A. Stimulation of the immune response during blockade of serotonin receptors by cyproheptadine. Biull Eksp Biol Med. 103:1987;440-442.
24. Ignatowski T.A., Spengler R.N. Tumor necrosis factor. Presynaptic sensitivity is modified after antidepressant drug administration Brain Res. 665:1994;293-299.
25. Jackson J.C., Walker R., Brooks W.H., Roszman T.L. Specific uptake of serotonin by murine macrophages. Life Sci. 42:1988;641-650.
26. Jahnova E. The role of serotonin in the regulation of the immune response. Bratisl Lek Listy. 95:1994;181-184.
27. Joyce P.R., Hawes C.R., Mulder R.T., Sellman J.D., Wilson D.A., Boswell D.R. Elevated levels of acute phase plasma proteins in major depression. Biol Psychiatry. 32:1992;1035-1041.
28. Katsikis P.D., Cohen S.B., Londei M., Feldmann M. Are CD4+ TH1 cells pro-inflammatory or anti-inflammatory? The ratio of IL-10 to IFN-gamma or IL-2 determines their function. Int Immunol. 7:1995;1287-1294.
29. 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. 48:1996;503-506.
30. Kubera M., Holan V., Basta-Kaim A., Roman A., Borycz J., Shani J. Effect of desipramine on immunological parameters in mice, and their reversal by stress. J Immunopharmacol. in press:1998.
31. Kut J.L., Young M.R., Crayton J.W., Wright M.A., Young M.E. Regulation of murine T-lymphocyte function by spleen cell-derivated and exogenous serotonin. Immunopharmacol Immunotoxicol. 14:1992;783-796.
32. Lieb K., Fiebich B.L., Busse-Grawitz M., Hull M., Berger M., Bauer J. Effects of substance P and selected other neuropeptides on the synthesis of interleukin-1 beta and interleukin-6 in human monocytes. A re-examination J Neuroimmunol. 67:1996;77-81.
33. Linnoila M., Whorton R., Rubinow D.R., Cowdry R.W., Ninan P.T., Waters R.N. CSF prostaglandin levels in depressed and schizophrenic patients. Arch Gen Psychiatry. 40:1983;405-406.
34. McDonald E.M., Mann A.H., Thomas H.C. Interferons as mediators of psychiatric morbidity. An investigation in a trial of recombinant α-interferon in hepatitis-B carriers Lancet. 2:1987;1175-1179.
35. McLoughlin I.J., Hodge J.S. Zinc in depressive disorder. Acta Psychiatr Scand. 82:1990;451-453.
36. Maes M (1997): The immune pathophysiology of major depression. In Honig A, van Praag H (eds), Depression: Neurobiological, Psychopathological and Therapeutic Advances. Chichester, John Wiley, pp 197-215.
37. Maes M., Meltzer H.Y.M. The serotonin hypothesis of major depression. Bloom F.E., Kupfer D.J. Psychopharmacology, the Fourth Generation of Progress. 1995;933-944 Raven Press, New York.
38. Maes M., Lambrechts J., Bosmans E., Jacobs J., Suy E., Vandervorst C., DeJonckheere C., Minner B., Raus J. Evidence for a systemic immune activation during depression. Results of leukocyte enumeration by flow cytometry in conjunction with monoclonal antibody staining Psychol Med. 22:1992;45-53.
39. Maes M., Bosmans E., Meltzer H.Y., Scharpé S., Suy E. Interleukin-1β A putative mediator of HPA-axis hyperactivity in major depression? Am J Psychiatry. 150:1993;1189-1193. a.
40. Maes M., Scharpé S., Meltzer H.Y., Bosmans E., Suy E., Calabrese J., Cosyns P. Relationships between interleukin-6 activity, acute phase proteins and HPA-axis function in severe depression. Psychiatr Res. 49:1993;11-27. b.
41. Maes M., Stevens W., Declerck L., Bridts C., Peeters D., Schotte C., Cosyns P. A significantly increased expression of T cell activation markers in depression. Additional evidence for an inflammatory process during that illness Prog Neuropsychopharmacol Biol Psychiatry. 17:1993;214-255. c.
42. Maes M., Scharpé S., Meltzer H.Y., Okayli G., Bosmans E., D'Hondt P., Vanden Bossche B., Cosyns P. Increased neopterin and interferon γ secretion and lower availability of L-tryptophan in major depression. Further evidence for activation of cell-mediated immunity Psychiatr Res. 54:1994;143-160.
43. Maes M., Meltzer H.Y., Bosmans E., Bergmans R., Vandoolaeghe E., Ranjan R., Desnyder R. Increased plasma concentrations of interleukin-6, soluble interleukin-6, soluble interleukin-2 and transferrin receptor in major depression. J Affect Disord. 34:1995;301-309. a.
44. Maes M., Smith R., Scharpe S. The monocyte-T lymphocyte hypothesis of major depression. Psychoneuroendocrinology. 20:1995;111-116. b.
45. Maes M, Delange J, Ranjan R, Meltzer HY, Desnyder R, Cooremans W, Scharpé S (1997a): Acute phase proteins in schizophrenia, mania and major depression: modulation by psychotropic drugs. Psychiatr Res 66:1-11.
46. Maes M, Song C, Lin A, Gabriels L, DeJongh R, Van Gastel A, Kenis G, Bosmans E, DeMeester I, Benoyt I, Neels H, Demedts P, Janca A, Scharpe S, Smith RS (1998a): The effects of psychological stress on humans: Increased production of proinflammatory cytokines and a Th-1-like response in stress-induced anxiety. Cytokine 10:313-318.
47. Maes M., Vandoolaeghe E., Neels H., Demedts P., Wauters A., Meltzer H.Y., Altamura C., Desnyder R. Lower serum zinc in major depression is a sensitive marker of treatment resistance and of the immune/inflammatory response in that illness. Biol Psychiatry. in press:1997;. b.
48. Maes M, Song C, Lin A, DeJongh R, Kenis G, Bosmans E, DeMeester I, Neels H, Scharpe S (1998b): Immune and clinical correlates of psychological stress-induced production of interferon-γ and IL-10 in humans. In Plotnikoff NP (ed), Cytokines, Stress and Immunity. In press.
49. Miller A.H., Lackner C. Tricyclic antidepressants and immunity. Miller A.H. Depressive Disorders and Immunity. 1989;85-104 American Psychiatric Press, Washington, DC.
50. Muller N., Hofschuste E., Ackenheil M., Mempel W., Eckstein R. Investigations of the cellular immunity during depression and the free interval. Evidence for an immune activation in affective psychosis Prog Neuropsychopharmacol Biol Psychiatry. 17:1993;713-730.
51. Nahas G.G., Desoize B., Leger C. Effects of psychotropic drugs on DNA synthesis in cultured lymphocytes (40447). Proc Soc Exp Biol Med. 160:1979;344-348.
52. Nassberger L., Traskman-Bendz L. Increased soluble interleukin-2 receptor concentrations in suicide attempters. Acta Psychiatr Scand. 88:1993;48-52.
53. Nordlind K., Sundstrom E., Bondesson L. Inhibiting effects of serotonin antagonists on the proliferation of mercuric chloride stimulated human peripheral blood T lymphocytes. Int Arch Allergy Immunol. 97:1992;105-108.
54. Perini G.I., Zara M., Carraro C., Tosin C., Gava F., Santucci M.G., Valverde S., Defranchis G. Psychoimmunoendocrine effects of panic disorder. Hum Psychopharmacol. 10:1995;461-465.
55. Pettipher E.R., Labasi J.M., Salter E.D., Stam E.J., Cheng J.B., Griffiths R.J. Regulation of tumor necrosis factor production by adrenal hormones in vivo. Insights into the anti-inflammatory activity of rolipram Br J Pharmacol. 117:1996;1530-1534.
56. Seidel A., Arolt V., Hunstiger M., Rink L., Behnisch A., Kirchner H. Cytokine production and serum proteins in depression. Scand J Immunol. 41:1995;534-538.
57. 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. a.
58. Seidel A., Arolt V., Hunstiger M., Rink L., Behnisch A., Kirchner H. Major depressive disorder is associated with elevated monocyte counts. Acta Psychiatr Scand. 94:1996;198-204. b.
59. Shirayama Y., Mitsushio H., Takashima M., Ichikawa H., Takahashi K. Reduction of substance P after chronic antidepressants treatment in the striatum, substantia nigra and amygdala of the rat. Brain Res. 739:1996;70-78.
60. Sluzewska A, Nowakowska E, Gryska K, Mackiewicz A (1994): Haptoglobin levels in a chronic mild stress model of depression in rats before and after treatment. Europ Neuropharmacol P-1-18:302.
61. Sluzewska A., Rybakowski J.K., Laciak M., Mackiewicz A., Sobieska M., Wiktorowiz K. Interleukin-6 serum levels in depressed patients before and after treatment with fluoxetine. Ann NY Acad Sci. 762:1995;474-476. a.
62. Sluzewska A., Rybakowski J., Bosmans E., Sobieska M., Berghmans R., Maes M., Wiktorowicz K. Indicators of immune activation in major depression. Psychiatr Res. 64:1996;161-167. a.
63. Sluzewska A., Rybakowski J.K., Sobieska M., Wiktorowicz K. Concentrations and microheterogeneity glycophorms of alpha-1-acid glycoprotein in major depression. J Affect Disord. 39:1996;149-155. b.
64. Sluzewska A., Rybakowski J.K., Sobieska M., Bosmans E., Pollet H., Wiktorowicz K. Increased levels of alpha-1-acid glycoprotein and interleukin-6 in refractory depression. Depression. 3:1995;170-175. b.
65. Smejkal-Jagar L., Boranic M. Serotonin, serotonergic agents and their antagonists suppress humoral immune reaction in vitro. Res Exp Med Berl. 194:1994;297-304.
66. Smith R.S. The macrophage theory of depression. Med Hypotheses. 35:1991;298-306.
67. Sommer N., Loschmann P.A., Northoff G.H., Weller M., Steinbrechter A., Steinbach J.P., Lichtenfels R., Meyermann R., Riethmuller A., Fontana A.et al. The antidepressant rolipram suppresses cytokine production and prevents autoimmune encephalomyelitis. Nature Med. 1:1995;244-248.
68. Song C., Leonard B.E. An acute phase protein response in the olfactory bulbectomized rat. Effect of sertraline treatment Med Sci Res. 22:1994;313-314.
69. Song C., Dinan T., Leonard B.E. Changes in immunoglobulin, complement and acute phase protein levels in the depressed patients and normal controls. J Affect Disord. 30:1994;283-288.
70. Sternberg E.M., Trial J., Parker C.W. Effects of serotonin on murine macrophages. Suppression of Ia expression by serotonin and its reversal by 5-HT2 serotonergic receptor antagonists J Immunol. 137:1986;276.
71. Suzuki E., Shintani F., Kanba S., Asai M., Nakaki T. Induction of interleukin-1 and interleukin-1 receptor antagonist mRNA by chronic treatment with various psychotropics in widespread area of rat brain. Neurosci Lett. 215:1996;201-204.
72. Swartz C.M. Albumin decrement in depression and cholesterol decrement in mania. J Affect Disord. 19:1990;173-176.
73. Weinberg S.B., Schulteis G., Fernando A.G., Bakhit C., Martinez J.L. Decreased locomotor activity produced by repeated, but not single, administration of murine-recombinant interferon-gamma in mice. Life Sci. 42:1988;1085-1090.
74. 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. Immunopharmacol. 34:1996;27-37.
75. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 711:1996;163-174.
76. Yirmiya R. Behavioral and psychological effects of immune activation. Implications for depression due to a general medical condition Curr Opinion Psychiatry. 10:1997;470-476.
77. Young M.R., Matthews J.P. Serotonin regulation of T cell subpopulations and of macrophage accessory function. Immunol. 84:1995;148-152.
78. Zangerle P.F., De Groote D., Lopez M., Meuleman R.J., Vrindts Y., Fauchet F., Dehart I., Jadoul M., Radoux D., Franchimont P. Direct stimulation of cytokines (IL-1 beta, TNF-alpha, IL-6, IL-2, IFN-gamma and GM-CSF) in whole blood. II. Application to rheumatoid arthritis and osteoarthritis Cytokine. 4:1992;568-575.