Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters

Neuropsychopharmacology

Volumn 35, Issue 13, 2010, Pages 2510-2520

  Zhu, Chong Bin ^a   Lindler, Kathryn M ^a   Owens, Anthony W ^b   Daws, Lynette C ^b   Blakely, Randy D ^a   Hewlett, William A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

depression; IL 1 receptor; lipopolysaccharide; p38 MAPK; serotonin transporter

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; INTERLEUKIN 1 RECEPTOR; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; FORCED SWIMMING TEST; HIPPOCAMPUS; HOPELESSNESS; IMMOBILIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DEPRESSION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; IMIDAZOLES; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RECEPTORS, INTERLEUKIN-1; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SYNAPTOSOMES;

EID: 78149466027     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.116     Document Type: Article

References (68)

1. Ait-Daoud N, Roache JD, Dawes MA, Liu L, Wang XQ, Javors MA et al (2009). Can serotonin transporter genotype predict craving in alcoholism? Alcohol Clin Exp Res 33: 1329-1335.
2. Anisman H (2009). Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder. J Psychiatry Neurosci 34: 4-20.
3. Apparsundaram S, Sung U, Price RD, Blakely RD (2001). Trafficking-dependent and-independent pathways of neuro-transmitter transporter regulation differentially involving p38 mitogen-activated protein kinase revealed in studies of insulin modulation of norepinephrine transport in SK-N-SH cells. J Pharmacol Exp Ther 299: 666-677.
4. Arakawa H, Blandino Jr P, Deak T (2009). Central infusion of interleukin-1 receptor antagonist blocks the reduction in social behavior produced by prior stressor exposure. Physiol Behav 98: 139-146.
5. Baganz NL, Horton RE, Calderon AS, Owens WA, Munn JL, Watts LT et al (2008). Organic cation transporter 3: Keeping the brake on extracellular serotonin in serotonin-transporter-deficient mice. Proc Natl Acad Sci USA 105: 18976-18981.
6. Bencsics A, Elenkov IJ, Vizi ES (1995). Alpha 2-, alpha 2A-, alpha 2B/2C-adrenoceptor subtype antagonists prevent lipopolysac-charide-induced fever response in rabbits. Brain Res 705: 302-306.
7. Blakely RD, Defelice LJ, Galli A (2005). Biogenic amine neuro-transmitter transporters: just when you thought you knew them. Physiology (Bethesda) 20: 225-231.
8. Capuron L, Dantzer R (2003). Cytokines and depression: the need for a new paradigm. Brain Behav Immun 17(Suppl 1): S119-S124.
9. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H et al (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301: 386-389.
10. Castanon N, Bluthé RM, Dantzer R (2001). Chronic treatment with the atypical antidepressant tianeptine attenuates sickness behavior induced by peripheral but not central lipopolysacchar-ide and interleukin-1beta in the rat. Psychopharmacology (Berl) 154: 50-60.
11. Castanon N, Konsman JP, Medina C et al (2003). Chronic treatment with the antidepressant tianeptine attenuates lipopo-lysaccharide-induced Fos expression in the rat paraventricular nucleus and HPA axis activation. Psychoneuroendocrinology 28: 19-34.
12. Chen R, Zhou H, Beltran J, Malellari L, Chang SL (2005). Differential expression of cytokines in the brain and serum during endotoxin tolerance. J Neuroimmunol 163: 53-72.
13. Cryan JF, Mombereau C, Vassout A (2005). The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 29: 571-625.
14. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9: 46-56.
15. Daws LC, Toney GM (2007). High-Speed Chronoamperometry to Study Kinetics and Mechanisms for Serotonin Clearance In Vivo. CRC Press, Taylor & Francis Group: Boca Raton, FL.
16. Diniz BS, Teixeira AL, Talib L, Gattaz WF, Forlenza OV (2010). Interleukin-1beta serum levels is increased in antidepressant-free elderly depressed patients. Am J Geriatr Psychiatry 8: 172-176.
17. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK et al (2010). A meta-analysis of cytokines in major depression. Biol Psychiatry 67: 446-457. Epub 2009 Dec 16.
18. Dunn AJ (2006). Effects of cytokines and infections on brain neurochemistry. Clin Neurosci Res 6: 52-68.
19. Dunn AJ, Swiergiel AH (2005). Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol Biochem Behav 81: 688-693.
20. Firk C, Markus CR (2007). Serotonin by stress interaction: a susceptibility factor for the development of depression? J Psychopharmacol 21: 538-544.
21. Gaspar P, Cases O, Maroteaux L (2003). The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4: 1002-1012.
22. Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T et al (2008). Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry 13: 717-728.
23. Gottschall PE, Komaki G, Arimura A (1992). Increased circulating interleukin-1 and interleukin-6 after intracerebroventricular injection of lipopolysaccharide. Neuroendocrinology 56: 935-938.
24. Guo AL, Petraglia F, Criscuolo M, Ficarra G, Salvestroni C, Nappi RE et al (1996). Adrenergic and serotoninergic receptors mediate the immunological activation of corticosterone secretion in male rats. Gynecol Endocrinol 10: 149-154.
25. Hall SR, Smith AP (1996). Behavioural effects of infectious mononucleosis. Neuropsychobiology 33: 202-209.
26. Hollis JH, Evans AK, Bruce KP, Lightman SL, Lowry CA (2006). Lipopolysaccharide has indomethacin-sensitive actions on Fos expression in topographically organized sub-populations of serotonergic neurons. Brain Behav Immun 20: 569-577.
27. Howren MB, Lamkin DM, Suls J (2009). Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med 71: 171-186. Epub 2009 Feb 2.
28. Katafuchi T, Kondo T, Take S, Yoshimura M (2005). Enhanced expression of brain interferon-alpha and serotonin transporter in immunologically induced fatigue in rats. Eur J Neurosci 22: 2817-2826.
29. Katafuchi T, Kondo T, Take S, Yoshimura M (2006). Brain cytokines and the 5-HT system during poly I:C-induced fatigue. Ann N Y Acad Sci 1088: 230-237. (Pubitemid 47092041)
30. Konsman JP, Veeneman J, Combe C, Poole S, Luheshi GN, Dantzer R (2008). Central nervous action of interleukin-1 mediates activation of limbic structures and behavioural depression in response to peripheral administration of bacterial lipopolysac-charide. Eur J Neurosci 28: 2499-2510.
31. Koo JW, Duman RS (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA 105: 751-756.
32. Koo JW, Duman RS (2009). Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression. Curr Opin Investig Drugs 10: 664-671.
33. Koo JW, Duman RS (2009). Interleukin-1 receptor null mutant mice show decreased anxiety-like behavior and enhanced fear memory. Neurosci Lett 456: 39-43.
34. Laucht M, Treutlein J, Blomeyer D, Buchmann AF, Schmid B, Becker K et al (2009). Interaction between the 5-HTTLPR serotonin transporter polymorphism and environmental adversity for mood and anxiety psychopathology: evidence from a high-risk community sample of young adults. Int J Neuro-psychopharmacol 12: 737-747.
35. Lavicky J, Dunn AJ (1994). Endotoxin administration stimulates cerebral catecholamine release in freely moving rats as assessed by microdialysis. J Neurosci Res 40: 407-413.
36. Lesch K-P (2001). Serotonergic gene expression and depression: implications for developing novel antidepressants. J Affect Disord 62: 57-76.
37. Levine J, Barak Y, Chengappa KN, Rapoport A, Rebey M, Barak V (1999). Cerebrospinal cytokine levels in patients with acute depression. Neuropsychobiology 40: 171-176. (Pubitemid 29515729)
38. Loppnow H, Libby P, Freudenberg M, Krauss JH, Weckesser J, Mayer H (1990). Cytokine induction by lipopolysaccharide (LPS) corresponds to lethal toxicity and is inhibited by nontoxic Rhodobacter capsulatus LPS. Infect Immun 58: 3743-3750.
39. Maes M (1999). Major depression and activation of the inflammatory response system. Adv Exp Med Biol 461: 25-46.
40. Maier SF, Watkins KT (1995). Intracerebroventricular interleukin-1 receptor antagonist blocks the enhancement of fear conditioning and interference with escape produced by inescapable shock. Brain Res 695: 279-286.
41. Meijer A, Zakay-Rones Z, Morag A (1988). Post-influenzal psychiatric disorder in adolescents. Acta Psychiatr Scand 78: 176-181.
42. Minor TR, Huang Q, Witt AE (2006). Cytokine-purine interactions in traumatic stress, behavioral depression, and sickness. CNS Neurol Disord Drug Targets 5: 547-560.
43. Mössner R, Daniel S, Schmitt A, Albert D, Lesch KP (2001). Modulation of serotonin transporter function by interleukin-4. Life Sci 68: 873-880.
44. Mössner R, Heils A, Stöber G, Okladnova O, Daniel S, Lesch KP (1998). Enhancement of serotonin transporter function by tumor necrosis factor alpha but not by interleukin-6. Neurochem Int 33: 251-254.
45. Müller N, Schwarz MJ (2007). The immune-mediated alteration of serotonin and glutamate: towards an integrated view of depression. Mol Psychiatry 12: 988-1000.
46. O'Connor JC, Lawson MA, André C, Moreau M, Lestage J, Castanon N et al (2009). Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry 14: 511-522.
47. Owen BM, Eccleston D, Ferrier IN, Young AH (2001). Raised levels of plasma interleukin-1beta in major and postviral depression. Acta Psychiatr Scand 103: 226-228.
48. Ozaki N, Goldman D, Kaye WH, Plotnicov K, Greenberg BD, Lappalainen J et al (2003). Serotonin transporter missense mutation associated with a complex neuropsychiatric pheno-type. Mol Psychiatry 8: 933-936. (Pubitemid 37421700)
49. Plata-Salamán CR, Borkoski JP (1993). Centrally administered bacterial lipopolysaccharide depresses feeding in rats. Pharmacol Biochem Behav 46: 787-791.
50. Pollak Y, Ovadia H, Goshen I, Gurevich R, Monsa K, Avitsur R et al (2000). Behavioral aspects of experimental autoimmune ence-phalomyelitis. J Neuroimmunol 104: 31-36.
51. Prasad HC, Steiner JA, Sutcliffe JS, Blakely RD (2009). Enhanced activity of human serotonin transporter variants associated with autism. Philos Trans R Soc Lond B Biol Sci 364: 163-173.
52. Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT (2008). Increased systemic and brain cytokine production and neuroin-flammation by endotoxin following ethanol treatment. J Neuroinflammation 5: 10.
53. Raison CL, Capuron L, Miller AH (2006). Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 27: 24-31.
54. Ramamoorthy S, Ramamoorthy JD, Prasad PD, Bhat GK, Mahesh VB, Leibach FH et al (1995). Regulation of the human serotonin transporter by interleukin-1 beta. Biochem Biophys Res Commun 216: 560-567.
55. Samuvel DJ, Jayanthi LD, Bhat NR, Ramamoorthy S (2005). A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J Neurosci 25: 29-41.
56. Schmitt A, Mössner R, Gossmann A, Fischer IG, Gorboulev V, Murphy DL et al (2003). Organic cation transporter capable of transporting serotonin is up-regulated in serotonin transporter-deficient mice. J Neurosci Res 71: 701-709.
57. Segal J, Schenkel LC, Oliveira MH, Salum GA, Bau CH, Manfro GG et al (2009). Novel allelic variants in the human serotonin transporter gene linked polymorphism (5-HTTLPR) among depressed patients with suicide attempt. Neurosci Lett 451: 79-82.
58. Swiergiel AH, Dunn AJ (2007). Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol Biochem Behav 86: 651-659.
59. Tuglu C, Kara SH, Caliyurt O, Vardar E, Abay E (2003). Increased serum tumor necrosis factor-alpha levels and treatment response in major depressive disorder. Psychopharmacology (Berl) 170: 429-433.
60. Van Den Biggelaar AH, Gussekloo J, de Craen AJ, Frölich M, Stek ML, van der Mast RC et al (2007). Inflammation and interleukin-1 signaling network contribute to depressive symptoms but not cognitive decline in old age. Exp Gerontol 42: 693-701.
61. Vaswani M, Linda FK, Ramesh S (2003). Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review. Prog Neuropsychopharmacol Biol Psychiatry 27: 85-102.
62. Vergne DE, Nemeroff CB (2006). The interaction of serotonin transporter gene polymorphisms and early adverse life events on vulnerability for major depression. Curr Psychiatry Rep 8: 447-452.
63. Yirmiya R (1996). Endotoxin produces a depressive-like episode in rats. Brain Res 711: 163-174.
64. Yirmiya R, Pollak Y, Barak O, Avitsur R, Ovadia H, Bette M et al (2001). Effects of antidepressant drugs on the behavioral and physiological responses to lipopolysaccharide (LPS) in rodents. Neuropsychopharmacology 24: 531-544.
65. Yirmiya R, Pollak Y, Morag M, Reichenberg A, Barak O, Avitsur R et al (2000). Illness, cytokines, and depression. Ann N Y Acad Sci 917: 478-487.
66. Yirmiya R, Weidenfeld J, Pollak Y, Morag M, Morag A, Avitsur R et al (1999). Cytokines, 'depression due to a general medical condition,' and antidepressant drugs. Adv Exp Med Biol 461: 283-316.
67. Zhu CB, Carneiro AM, Dostmann WR, Hewlett WA, Blakely RD (2005). p38 MAPK activation elevates serotonin transport activity via a trafficking-independent, protein phosphatase 2A-dependent process. J Biol Chem 280: 15649-15658.
68. Zhu CB, Hewlett WA, Blakely RD (2006). The proinflammatory cytokines interleukine-1beta and tumor necrosis factor-alpha activate serotonin transporters. Neuropsychopharmacology 31: 2121-2131.