Time-dependent in-vivo effects of interleukin-2 on neurotransmitters in various cortices: Relationships with depressive-related and anxiety-like behaviour

Journal of Neuroimmunology

Volumn 237, Issue 1-2, 2011, Pages 23-32

  Karrenbauer, B D ^a   Muller C P ^b   Ho, Y J ^c   Spanagel, R ^d   Huston, J P ^e   Schwarting, R K W ^a   Pawlak, C R ^d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^e HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Anxiety; Cytokines; Depression; Forced swim test; HPLC EC; In vivo microdialysis

Indexed keywords

DOPAMINE; INTERLEUKIN 2; SEROTONIN; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BODY TEMPERATURE; BODY WEIGHT; BRAIN CORTEX; CONTROLLED STUDY; DEPRESSION; DOPAMINERGIC TRANSMISSION; DRUG DOSE COMPARISON; FORCED SWIMMING TEST; IN VIVO STUDY; MALE; MAZE TEST; MICRODIALYSIS; NONHUMAN; OCCIPITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEROTONINERGIC TRANSMISSION; TEMPORAL CORTEX; TIME;

ANIMALS; ANXIETY DISORDERS; CEREBRAL CORTEX; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; DOPAMINE; INTERLEUKIN-2; MALE; MICRODIALYSIS; RATS; RATS, WISTAR; SEROTONIN; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 80051475443     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.05.011     Document Type: Article

References (89)

1. Allgulander C., Nilsson B. A prospective study of 86 new patients with social anxiety disorder. Acta Psychiatr. Scand. 2001, 103:447-452.
2. Anisman H., Merali Z. Anhedonic and anxiogenic effects of cytokine exposure. Adv. Exp. Med. Biol. 1999, 461:199-233.
3. Anisman H., Kokkinidis L., Merali Z. Interleukin-2 decreases accumbal dopamine efflux and responding for rewarding lateral hypothalamic stimulation. Brain Res 1996, 731:1-11.
4. Anisman H., Kokkinidis L., Borowski T., Merali Z. Differential effects of interleukin (IL)-1beta, IL-2 and IL-6 on responding for rewarding lateral hypothalamic stimulation. Brain Res. 1998, 779:177-187.
5. Anisman H., Kokkinidis L., Merali Z. Further evidence for the depressive effects of cytokines: anhedonia and neurochemical changes. Brain Behav. Immun. 2002, 16:544-556.
6. Anisman H., Merali Z., Poulter M.O., Hayley S. Cytokines as a precipitant of depressive illness: animal and human studies. Curr. Pharm. Des. 2005, 11:963-972.
7. Baldwin D.S., Evans D.L., Hirschfeld R.M., Kasper S. Can we distinguish anxiety from depression?. Psychopharmacol. Bull. 2002, 36:158-165.
8. Bhatt S., Zalcman S., Hassanain M., Siegel A. Cytokine modulation of defensive rage behavior in the cat: role of GABAA and interleukin-2 receptors in the medial hypothalamus. Neuroscience 2005, 133:17-28.
9. Boix F., Sandor P., Nogueira P.J., Huston J.P., Schwarting R.K.W. Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region. Neuroscience 1995, 64:1045-1055.
10. Bonaccorso S., Marino V., Puzella A., Pasquini M., Biondi M., Artini M., Almerighi C., Verkerk R., Meltzer H., Maes M. Increased depressive ratings in patients with hepatitis C receiving interferon-alpha-based immunotherapy are related to interferon-alpha-induced changes in the serotonergic system. J. Clin. Psychopharmacol. 2002, 22:86-90.
11. Brown R.R., Lee C.M., Kohler P., Hank J.A., Storer B.E., Sondel P.M. Altered tryptophan and neopterin metabolism in cancer patients treated with recombinant interleukin 2. Cancer Res. 1989, 49:4941-4944.
12. Capuron L., Ravaud A., Dantzer R. Early depressive symptoms in cancer patients receiving interleukin 2 and/or interferon Alfa-2b therapy. J. Clin. Oncol. 2000, 18:2143-2151.
13. Capuron L., Ravaud A., Gualde N., Bosmans E., Dantzer R., Maes M., Neveu P.J. Association between immune activation and early depressive symptoms in cancer patients treated with interleukin-2-based therapy. Psychoneuroendocrinology 2001, 26:797-808.
14. Capuron L., Gumnick J.F., Musselman D.L., Lawson D.H., Reemsnyder A., Nemeroff C.B., Miller A.H. Neurobehavioral effects of interferon-α in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 2002, 26:643-652.
15. Capuron L., Hauser P., Hinze-Selch D., Miller A.H., Neveu P.J. Treatment of cytokine-induced depression. Brain Behav Immun 2002, 16:575-580.
16. Capuron L., Ravaud A., Neveu P.J., Miller A.H., Maes M., Dantzer R. Association between decreased serum tryptophan concentrations and depressive symptoms in cancer patients undergoing cytokine therapy. Mol. Psychiatry 2002, 7:468-473.
17. Capuron L., Neurauter G., Musselman D.L., Lawson D.H., Nemeroff C.B., Fuchs D., Miller A.H. Interferon-alpha-induced changes in tryptophan metabolism. relationship to depression and paroxetine treatment. Biol. Psychiatry 2003, 54:906-914.
18. Capuron L., Pagnoni G., Demetrashvili M.F., Lawson D.H., Fornwalt F.B., Woolwine B., Berns G.S., Nemeroff C.B., Miller A.H. Basal ganglia hypermetabolism and symptoms of fatigue during interferon-α therapy. Neuropsychopharmacology 2007, 32:2384-2392.
19. Carlin J.M., Borden E.C., Sondel P.M., Byrne G.I. Biologic-response-modifier-induced indoleamine 2,3-dioxygenase activity in human peripheral blood mononuclear cell cultures. J. Immunol. 1987, 139:2414-2418.
20. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20years on. Neurosci. Biobehav. Rev. 2005, 29:1193-1205.
21. Chen N.H., Reith M.E. Autoregulation and monoamine interactions in the ventral tegmental area in the absence and presence of cocaine: a microdialysis study in freely moving rats. J. Pharmacol. Exp. Ther. 1994, 271:1597-1610.
22. Connor T.J., Song C., Leonard B.E., Merali Z., Anisman H. An assessment of the effects of central interleukin-1β, -2, -6, and tumor necrosis factor-α administration on some behavioural, neurochemical, endocrine and immune parameters in the rat. Neuroscience 1998, 84:923-933.
23. Coppen A. The biochemistry of affective disorders. Brit. J. Psychiatry 1967, 119:1237-1264.
24. Cryan J.F., Markou A., Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci. 2002, 23:238-245.
25. Cummings J.L. The neuroanatomy of depression. J. Clin. Psychiatry 1993, 54:14-20.
26. Dantzer R., Bluthé R.M., Castanon N., Chauvet N., Capuron L., Goodall G., Kelley K.W., Konsman J.P., Layé S., Parnet P., Pousset F. Cytokine effects on behavior. Psychoneuroimmunology 2001, Vol. 1:703-727. Academic Press, San Diego. 3rd ed. R. Ader, D.L.,.F.N. Cohen (Eds.).
27. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. Form inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-57.
28. De Souza Silva M.A., Müller C.P., Huston J.P. Microdialysis in the brain of anesthetized vs. freely moving animals. Handbook of Microdialysis: Methods, Applications and Perspectives 2007, 71-92. Elsevier, Amsterdam. B. Westerink, T. Cremers (Eds.).
29. Drevets W.C., Price J.L., Simpson J.R.J., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386:824-827.
30. Dunn A.J., Swiergiel A.H. Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol. Biochem. Behav. 2005, 81:688-693.
31. Dunn A.J., Swiergiel A.H., de Beaurepaire R. Cytokines as mediator of depression: what can we learn from animal studies?. Neurosci. Biobehav. Rev. 2005, 29:891-909.
32. Enkel T., Gholizadeh D., von Bohlen und Halbach O., Sanchis-Segura C., Hurlemann R., Spanagel R., Gass P., Vollmayr B. Ambiguous-cue interpretation is biased under stress- and depression-like states in rats. Neuropsychopharmacology 2010, 35:1008-1015.
33. Figee M., Denys D. New pharmacotherapeutic approaches to obsessive-compulsive disorder. CNS Spectr. 2009, 14:13-23.
34. Frenois F., Moreau M., O' Connor J., Lawson M., Micon C., Lestage J., Kelley K.W., Dantzer R., Castanon N. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 2007, 32:516-531.
35. George M.S., Ketter T.A., Post R.M. SPECT and PET imaging in mood disorders. J. Clin. Psychiatry 1993, 54:6-13.
36. Hanisch U.K. Effects of Interleukin-2 and interferons on the nervous system. Psychoneuroimmunology 2001, Vol. 1:585-631. Academic Press, San Diego. 3rd ed. R. Ader, D.L. Felten, N. Cohen (Eds.).
37. Hart B.L. Biological basis of the behaviour of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
38. Hauser P., Khosla J., Aurora H., Laurin J., Kling M.A., Hill J., Gulati M., Thornton A.J., Schultz R.L., Valentine A.D., Meyers C.A., Howell C.D. A prospective study of the incidence and open-label treatment of interferon-induced major depressive disorder in patients with hepatitis C. Mol Psychiatry 2002, 7:942-947.
39. Hodos W., Kalman G. Effects of increment size and reinforcer volume on progressive ratio performance. J. Exp. Anal. Behav. 1963, 6:387-392.
40. Howell D.C. Statistical Methods for Psychology 1992, 338. Duxbury Press, Belmont. 3rd ed.
41. Juengling F.D., Ebert D., Gut O., Engelbrecht M.A., Rasenack J., Nitzsche E.U., Bauer J., Lieb K. Prefrontal cortical hypometabolism during low-dose interferon alpha treatment. Psychopharmacology 2000, 152:383-389.
42. Karrenbauer B.D., Ho Y.J., Ludwig V., Löhn J., Spanagel R., Schwarting R.K.W., Pawlak C.R. Time-dependent effects of striatal interleukin-2 on open field behaviour in rats. J. Neuroimmunol. 2009, 208:10-18.
43. Kent J.M., Coplan J.D., Gorman J.M. Clinical utility of the selective serotonin reuptake inhibitors in the spectrum of anxiety. Biol. Psychiatry 1998, 44:812-824.
44. Kiecolt-Glaser J.K., McGuire L., Robles T.F., Glaser R. Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology. Annu. Rev. Psychol. 2002, 53:83-107.
45. Kim Y.K., Jung H.G., Myint A.M., Kim H., Park S.H. Imbalance between pro-inflammatory and anti-inflammatory cytokines in bipolar disorder. J. Affect. Disord. 2007, 104:91-95.
46. Lacosta S., Merali Z., Anisman H. Influence of acute and repeated interleukin-2 administration on spatial learning, locomotor activity, exploratory behaviors, and anxiety. Behav. Neurosci. 1999, 113:1030-1041.
47. Lacosta S., Merali Z., Anisman H. Central monoamine activity following acute and repeated systemic interleukin-2 administration. Neuroimmunomodulation 2000, 8:83-90.
48. Leonard B.E. The immune system, depression and the action of antidepressants. Prog. Neuropsychopharmacol. Biol. Psychiatry 2001, 25:767-780.
49. Lesperance F., Frasure-Smith N., Théroux P., Irwin M. The association between major depression and levels of soluble intercellular adhesion molecule 1, interleukin 6, and C-reactive protein in patients with recent acute coronary syndromes. Am. J. Psychiatry 2004, 161:271-277.
50. Lissoni P., Rovelli F., Brivio F., Brivio O., Fumagalli L. Circadian secretions of IL-2, IL-12, IL-6 and IL-10 in relation to the light/dark rhythm of the pineal hormone melatonin in healthy humans. Nat. Immun. 1998, 16:1-5.
51. Marques-Deak A.H., Lotufo Neto F., Dominguez W.V., Solis A.C., Kurcgant D., Sato F., Ross J.M., Prado E.B.A. Cytokines profiles in women with different subtypes of major depressive disorders. J. Psychiatr. Res. 2007, 41:152-159.
52. Miguelez M., Lacasse M., Kentner A.C., Rizk I., Fouriezos G., Bielajew C. Short- and long-term effects of interleukin-2 on weight, food intake, and hedonic mechanisms in the rat. Behav. Brain Res. 2004, 154:311-319.
53. Miura H., Ozaki N., Sawada M., Isobe K., Ohta T., Nagatsu T. A link between stress and depression: shifts in the balance between the kynurenine and serotonin pathways of tryptophan metabolism and the etiology and pathophysiology of depression. Stress 2008, 11:198-209.
54. Montkowski A., Landgraf R., Yassouridis A., Holsboer F., Schobitz B. Central administration of IL-1 reduces anxiety and induces sickness behaviour in rats. Pharmacol. Biochem. Behav. 1997, 58:329-336.
55. Morikawa O., Sakai N., Obara H., Saito N. Effects of interferon-alpha, interferon-gamma and cAMP on the transcriptional regulation of the serotonin transporter. Eur. J. Pharmacol. 1998, 349:317-324.
56. Mössner R., Heils A., Stober G., Okladnova O., Daniel S., Lesch K.P. Enhancement of serotonin transporter function by tumor necrosis factor alpha but not by interleukin-6. Neurochem. Int. 1998, 33:251-254.
57. Müller C.P., De Souza Silva M.A., Huston J.P. Double dissociating effects of sensory stimulation and cocaine on serotonin activity in the occipital and temporal cortices. Neuropharmacology 2007, 52:854-862.
58. Musselman D.L., Lawson D.H., Gumnick J.F., Manatunga A.K., Penna S., Goodkin R.S., Greiner K., Nemeroff C.B., Miller A.H. Paroxetine for the prevention of depression induced by high-dose interferon alfa. N. Engl. J. Med. 2001, 344:961-966.
59. Myint A.M., Leonard B.E., Steinbusch H.W., Kim Y.K. Th1, Th2, and Th3 cytokine alterations in major depression. J. Affect. Disord. 2005, 88:167-173.
60. 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 1991, 104:255-259.
61. Pauli S., Linthorst A.C.E., Reul J.M.H.M. Tumour necrosis factor-α and interleukin-2 differentially affect hippocampal serotonergic neurotransmission, behavioural activity, body temperature and hypothalamic-pituitary-adrenocortical axis activity in the rat. Eur. J. Neurosci. 1998, 10:868-878.
62. Pawlak C.R., Schwarting R.K.W. Striatal microinjections of interleukin-2 and rat behaviour in the elevated plus-maze. Behav Brain Res 2006, 168:339-344.
63. Pawlak C.R., Ho Y.J., Schwarting R.K.W., Bauhofer A. Relationship between striatal levels of interleukin-2 mRNA and plus-maze behaviour in the rat. Neurosci. Lett. 2003, 341:205-208.
64. Pawlak C.R., Schwarting R.K.W., Bauhofer A. Cytokine mRNA levels in brain and peripheral tissues of the rat: relationships with plus-maze behaviour. Mol. Brain Res. 2005, 137:159-165.
65. Paxinos G., Watson C. The Rat Brain in Stereotactic Coordinates 1986, Academic Press, Sydney. 2nd ed.
66. Petitto J.M., McCarthy D.B., Rinker C.M., Huang Z., Getty T. Modulation of behavioral and neurochemical measures of forebrain dopamine function in mice by species-specific interleukin-2. J. Neuroimmunol. 1997, 73:183-190.
67. Petitto J.M., Huang Z., Hartemink D.A., Beck R. IL-2/15 receptor-β gene deletion alters neurobehavioral performance. Brain Res 2002, 929:218-225.
68. Pollack M.H., Zaninelli R., Goddard A., McCafferty J.P., Bellew K.M., Burnham D.B., Iyengar M.K. Paroxetine in the treatment of generalized anxiety disorder: results of a placebo-controlled, flexible-dosage trial. J. Clin. Psychiatry 2001, 62:350-357.
69. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
70. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 1978, 47:379-391.
71. Pum M.E., De Huston J.P., Souza Silva M.A., Müller C.P. Visual sensory-motor gating by serotonin activation in the medial prefrontal and occipital, but not in the rhinal, cortices in rats. Neuroscience 2008, 153:361-372.
72. Ramamoorthy S., Ramamoorthy J.D., Prasad P.D., Bhat G.K., Mahesh V.B., Leibach F.H., Ganapathy V. Regulation of the human serotonin transporter by interleukin-1 beta. Biochem. Biophys. Res. Commun. 1995, 216:560-567.
73. Rapaport M.H., Stein M.B. Serum cytokine and soluble interleukine-2 receptors in patients with panic disorder. Anxiety 1994, 1:22-25.
74. Schatzberg A.F. New indications for antidepressants. J. Clin. Psychiatry 2000, 61:9-17.
75. Schneider M., Heise V., Spanagel R. Differential involvement of the opioid receptor antagonist naloxone in motivational and hedonistic aspects of reward. Behav Brain Res 2010, 208:466-472.
76. Schneider P., Weber-Fahr W., Leonardi-Essmann F., Spanagel R., Sartorius A., Pawlak C. Differential psychopharmacology: interleukin-2 effects on behaviour and neurochemistry. Program No. 297.11/III44. 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010. Online. Paper presented at the Society for Neuroscience, 40th Annual Meeting. San Diego, USA 2010.
77. Schruers K., Klaassen T., Pols H., Overbeek T., Deutz N.E., Griez E. Effects of tryptophan depletion on carbon dioxide provoked panic in panic disorder patients. Psychiatry Res. 2000, 93:179-187.
78. Schruers K., van Diest R., Overbeek T., Griez E. Acute l-5-hydroxytryptophan administration inhibits carbon dioxide-induced panic in panic disorder patients. Psychiatry Res 2002, 113:237-243.
79. Seidel A., Arolt V., Hunstiger M., Rink L., Behnisch A., Kirchner H. Cytokine production and serum proteins in depression. Scand. J. Immunol. 1995, 41:534-538.
80. Song C., Merali Z., Anisman H. Variations of nucleus accumbens dopamine and serotonin following systemic interleukin-1, interleukin-2 or interleukin-6 treatment. Neuroscience 1999, 88:823-836.
81. Steptoe A., Kunz-Ebrecht S.R., Owen N. Lack of association between depressive symptopms and markers of immune and vascular inflammation in middle-aged men and women. Psychol. Med. 2003, 33:667-674.
82. Tsao C.W., Lin Y.S., Chen C.C., Bai C.H., Wu S.R. Cytokines and serotonin transporter in patients with major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:899-905.
83. Vitkovic L., Bockaert J., Jacque C. "Inflammatory" cytokines: neuromodulators in normal brain?. J. Neurochem. 2000, 74:457-471.
84. Westenberg H.G. Developments in the drug treatment of panic disorder: what is the place of the selective serotonin reuptake inhibitors?. J. Affect. Disord. 1996, 40:85-93.
85. Wichers M., Maes M. The psychoneuroimmuno-pathophysiology of cytokine-induced depression in humans. Int. J. Neuropsychopharmacol. 2002, 5:375-388.
86. Wilcox R.R. New designs in analysis of variance. Annu. Rev. Psychol. 1987, 38:29-60.
87. Zalcman S.S. Interleukin-2 potentiates novelty- and GBR 12909-induced exploratory activity. Brain Res 2001, 899:1-9.
88. Zalcman S.S., Green-Johnson J.M., Murray L., Nance D.M., Dyck D., Anisman H., Greenberg A.H. Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6. Brain Res 1994, 643:40-49.
89. Zalcman S., Murray L., Dyck D.G., Greenberg A.H., Nance D.M. Interleukin-2 and -6 induce behavioral-activating effects in mice. Brain Res 1998, 811:111-121.