Lipopolysaccharide-induced anhedonia is abolished in male serotonin transporter knockout rats: An intracranial self-stimulation study

Brain, Behavior, and Immunity

Volumn 29, Issue , 2013, Pages 98-103

  Van Heesch, Floor ^a   Prins, Jolanda ^a   Konsman, Jan Pieter ^b   Westphal, Koen G C ^a   Olivier, Berend ^a   Kraneveld, Aletta D ^a   Korte, S Mechiel ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Anhedonia; Body weight; Depression; Intracranial self stimulation; Lipopolysaccharide; Serotonin transporter knockout

Indexed keywords

CARPROFEN; LIPOPOLYSACCHARIDE; SEROTONIN TRANSPORTER;

ANHEDONIA; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN SURGERY; CONTROLLED STUDY; ELECTRODE; GENOTYPE; HETEROZYGOTE; INFLAMMATION; LATENT PERIOD; MALE; MEDIAL FOREBRAIN BUNDLE; NONHUMAN; PRIORITY JOURNAL; RAT; SELF STIMULATION; WEIGHT;

ANALYSIS OF VARIANCE; ANHEDONIA; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AREA UNDER CURVE; BACTERIAL TOXINS; BODY WEIGHT; BRAIN; CYTOKINES; ENTEROTOXINS; GENE DELETION; LIPOPOLYSACCHARIDES; MALE; RATS; SELF STIMULATION; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84873432955     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.12.013     Document Type: Article

References (50)

1. Albert P.R., Benkelfat C., Descarries L. The neurobiology of depression-revisiting the serotonin hypothesis. I. Cellular and molecular mechanisms. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2012, 367:2378-2381.
2. Bode J.G., Ehlting C., Haussinger D. The macrophage response towards LPS and its control through the p38(MAPK)-STAT3 axis. Cell Signal. 2012, 24:1185-1194.
3. Borowski T., Kokkinidis L., Merali Z., Anisman H. Lipopolysaccharide, central in vivo biogenic amine variations, and anhedonia. Neuroreport 1998, 9:3797-3802.
4. Bull S.J., Huezo-Diaz P., Binder E.B., Cubells J.F., Ranjith G., Maddock C., Miyazaki C., Alexander N., Hotopf M., Cleare A.J., Norris S., Cassidy E., Aitchison K.J., Miller A.H., Pariante C.M. Functional polymorphisms in the interleukin-6 and serotonin transporter genes, and depression and fatigue induced by interferon-alpha and ribavirin treatment. Mol. Psychiatry. 2009, 14:1095-1104.
5. Capuron L., Gumnick J.F., Musselman D.L., Lawson D.H., Reemsnyder A., Nemeroff C.B., Miller A.H. Neurobehavioral effects of interferon-alpha in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 2002, 26:643-652.
6. Capuron L., Ravaud A., Miller A.H., Dantzer R. Baseline mood and psychosocial characteristics of patients developing depressive symptoms during interleukin-2 and/or interferon-alpha cancer therapy. Brain Behav. Immun. 2004, 18:205-213.
7. Cryan J.F., Hoyer D., Markou A. Withdrawal from chronic amphetamine induces depressive-like behavioral effects in rodents. Biol. Psychiatry. 2003, 54:49-58.
8. Dantzer R. Cytokine, sickness behavior, and depression. Immunol. Allergy Clin. North. Am. 2009, 29:247-264.
9. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
10. Diamond M., Kelly J.P., Connor T.J. Antidepressants suppress production of the Th1 cytokine interferon-gamma, independent of monoamine transporter blockade. Eur. Neuropsychopharmacol. 2006, 16:481-490.
11. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., Lanctot K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry. 2010, 67:446-457.
12. 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.
13. Galvao-de Almeida A., Guindalini C., Batista-Neves S., de Oliveira I.R., Miranda-Scippa A., Quarantini L.C. Can antidepressants prevent interferon-alpha-induced depression? A review of the literature. Gen. Hosp. Psychiatry. 2010, 32:401-405.
14. Hannestad J., DellaGioia N., Bloch M. The effect of antidepressant medication treatment on serum levels of inflammatory cytokines: a meta-analysis. Neuropsychopharmacology 2011, 36:2452-2459.
15. Heinze S., Egberts F., Rotzer S., Volkenandt M., Tilgen W., Linse R., Boettjer J., Vogt T., Spieth K., Eigentler T., Brockmeyer N.H., Hinzpeter A., Hauschild A., Schaefer M. Depressive mood changes and psychiatric symptoms during 12-month low-dose interferon-alpha treatment in patients with malignant melanoma: results from the multicenter DeCOG trial. J. Immunother. 2010, 33:106-114.
16. Homberg J.R., la Fleur S.E., Cuppen E. Serotonin transporter deficiency increases abdominal fat in female, but not male rats. Obesity (Silver Spring) 2010, 18:137-145.
17. Homberg J.R., Olivier J.D., Smits B.M., Mul J.D., Mudde J., Verheul M., Nieuwenhuizen O.F., Cools A.R., Ronken E., Cremers T., Schoffelmeer A.N., Ellenbroek B.A., Cuppen E. Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 2007, 146:1662-1676.
18. Hutson P.H., Donohoe T.P., Curzon G. Infusion of the 5-hydroxytryptamine agonists RU24969 and TFMPP into the paraventricular nucleus of the hypothalamus causes hypophagia. Psychopharmacology (Berl) 1988, 95:550-552.
19. Kaster M.P., Gadotti V.M., Calixto J.B., Santos A.R., Rodrigues A.L. Depressive-like behavior induced by tumor necrosis factor-alpha in mice. Neuropharmacology 2012, 62:419-426.
20. Kenny P.J., Markou A. Nicotine self-administration acutely activates brain reward systems and induces a long-lasting increase in reward sensitivity. Neuropsychopharmacology 2006, 31:1203-1211.
21. Kenny P.J., Polis I., Koob G.F., Markou A. Low dose cocaine self-administration transiently increases but high dose cocaine persistently decreases brain reward function in rats. Eur. J. Neurosci. 2003, 17:191-195.
22. Konsman J.P., Parnet P., Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 2002, 25:154-159.
23. Kornetsky C., Esposito R.U. Euphorigenic drugs: effects on the reward pathways of the brain. Fed. Proc. 1979, 38:2473-2476.
24. Kraus M.R., Al-Taie O., Schafer A., Pfersdorff M., Lesch K.P., Scheurlen M. Serotonin-1A receptor gene HTR1A variation predicts interferon-induced depression in chronic hepatitis C. Gastroenterology 2007, 132:1279-1286.
25. Kraus M.R., Schafer A., Faller H., Csef H., Scheurlen M. Paroxetine for the treatment of interferon-alpha-induced depression in chronic hepatitis C. Aliment. Pharmacol. Ther. 2002, 16:1091-1099.
26. Langhans W. Signals generating anorexia during acute illness. Proc. Nutr. Soc. 2007, 66:321-330.
27. Langhans W., Hrupka B. Interleukins and tumor necrosis factor as inhibitors of food intake. Neuropeptides 1999, 33:415-424.
28. Larson S.J. Lipopolysaccharide and interleukin-1beta decrease sucrose intake but do not affect expression of place preference in rats. Pharmacol. Biochem. Behav. 2006, 84:429-435.
29. Lee K.M., Kim Y.K. The role of IL-12 and TGF-beta1 in the pathophysiology of major depressive disorder. Int. Immunopharmacol. 2006, 6:1298-1304.
30. Lotrich F.E., Ferrell R.E., Rabinovitz M., Pollock B.G. Risk for depression during interferon-alpha treatment is affected by the serotonin transporter polymorphism. Biol. Psychiatry. 2009, 65:344-348.
31. Markou A., Koob G.F. Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol. Behav. 1992, 51:111-119.
32. McNutt M.D., Liu S., Manatunga A., Royster E.B., Raison C.L., Woolwine B.J., Demetrashvili M.F., Miller A.H., Musselman D.L. Neurobehavioral effects of interferon-alpha in patients with hepatitis-C: symptom dimensions and responsiveness to paroxetine. Neuropsychopharmacology 2012, 37:1444-1454.
33. Mossner 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.
34. Olivier J.D., Van Der Hart M.G., Van Swelm R.P., Dederen P.J., Homberg J.R., Cremers T., Deen P.M., Cuppen E., Cools A.R., Ellenbroek B.A. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 2008, 152:573-584.
35. Pellegrino L., Pellegrino A., Cushman A. A stereotaxic Atlas of the Rat Brain 1979, Plenum Press, New York.
36. Prins, J., van Heesch, F., de Haan, L., Krajnc, A.M., Kenny, P.J., Olivier, B., Kraneveld, A.D., Korte, S.M., 2011. Lipolysaccharide-induced changes in brain stimulation reward: anhedonia or sickness behaviour? Poster session presented at: ECNP 2010. ECNP Workshop on Neuropsychopharmacology for Young Scientists in Europe, March 4-7, 2010. Nice, France.
37. Prins J., Kenny P.J., Doomernik I., Schreiber R., Olivier B., Mechiel Korte S. The triple reuptake inhibitor DOV 216,303 induces long-lasting enhancement of brain reward activity as measured by intracranial self-stimulation in rats. Eur. J. Pharmacol. 2012, 693:51-56.
38. Raison C.L., Woolwine B.J., Demetrashvili M.F., Borisov A.S., Weinreib R., Staab J.P., Zajecka J.M., Bruno C.J., Henderson M.A., Reinus J.F., Evans D.L., Asnis G.M., Miller A.H. Paroxetine for prevention of depressive symptoms induced by interferon-alpha and ribavirin for hepatitis C. Aliment. Pharmacol. Ther. 2007, 25:1163-1174.
39. Renault P.F., Hoofnagle J.H., Park Y., Mullen K.D., Peters M., Jones D.B., Rustgi V., Jones E.A. Psychiatric complications of long-term interferon alfa therapy. Arch. Intern. Med. 1987, 147:1577-1580.
40. Schwartz D., Hernandez L., Hoebel B.G. Fenfluramine administered systemically or locally increases extracellular serotonin in the lateral hypothalamus as measured by microdialysis. Brain Res. 1989, 482:261-270.
41. Smits B.M., Mudde J.B., van de Belt J., Verheul M., Olivier J., Homberg J., Guryev V., Cools A.R., Ellenbroek B.A., Plasterk R.H., Cuppen E. Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenet. Genomics 2006, 16:159-169.
42. Stoker A., Markou A. The intracranial self-stimulation procedure provides quantitative measures of brain reward function. Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests 2011, Vol. II:307. Springer.
43. Sutcigil L., Oktenli C., Musabak U., Bozkurt A., Cansever A., Uzun O., Sanisoglu S.Y., Yesilova Z., Ozmenler N., Ozsahin A., Sengul A. Pro- and anti-inflammatory cytokine balance in major depression: effect of sertraline therapy. Clin. Dev. Immunol. 2007, 2007:76396.
44. Taler M., Gil-Ad I., Lomnitski L., Korov I., Baharav E., Bar M., Zolokov A., Weizman A. Immunomodulatory effect of selective serotonin reuptake inhibitors (SSRIs) on human T lymphocyte function and gene expression. Eur. Neuropsychopharmacol. 2007, 17:774-780.
45. Tsao C.W., Lin Y.S., Cheng J.T., Lin C.F., Wu H.T., Wu S.R., Tsai W.H. Interferon-alpha-induced serotonin uptake in Jurkat T cells via mitogen-activated protein kinase and transcriptional regulation of the serotonin transporter. J. Psychopharmacol. 2008, 22:753-760.
46. van Heesch, F., Prins, J., Westphal, K.G.C., Korte-Bouws, G.A.H., Hoevenaar, W.H.M., Olivier, B., Kraneveld, S.M., Korte, S.M., 2012. Pro-inflammatory cytokines affect monoamine (metabolite) levels in the nucleus accumbens and induce anhedonia in mice. Poster session presented at: SfN Neuroscience 2012. 42nd Annual Meeting of SFN Neuroscience, October13-17, 2012. New Orleans, USA.
47. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 1996, 711:163-174.
48. Zhu C.B., Blakely R.D., Hewlett W.A. The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-alpha activate serotonin transporters. Neuropsychopharmacology 2006, 31:2121-2131.
49. Zhu C.B., Hewlett W.A., Feoktistov I., Biaggioni I., Blakely R.D. Adenosine receptor, protein kinase G, and p38 mitogen-activated protein kinase-dependent up-regulation of serotonin transporters involves both transporter trafficking and activation. Mol. Pharmacol. 2004, 65:1462-1474.
50. Zhu C.B., Lindler K.M., Owens A.W., Daws L.C., Blakely R.D., Hewlett W.A. Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacology 2010, 35:2510-2520.