A requirement of serotonergic p38α mitogen-Activated protein kinase for peripheral immune system activation of CNS serotonin uptake and serotonin-linked behaviors

Translational Psychiatry

Volumn 5, Issue , 2015, Pages

  Baganz, N L ^a   Lindler, K M ^a   Zhu, C B ^b   Smith, J T ^a   Robson, M J ^a   Iwamoto, H ^a   Deneris, E S ^c   Hewlett, W A ^d   Blakely, R D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d Institute for Psychiatric Neuroscience   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 14; SEROTONIN; SEROTONIN TRANSPORTER; TUMOR NECROSIS FACTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; BRAIN SYNAPTOSOME; CELL VIABILITY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG CLEARANCE; ELEVATED PLUS MAZE TEST; FORCED SWIM TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNATE IMMUNITY; LIQUID CHROMATOGRAPHY; LOCOMOTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SEROTONIN UPTAKE; ANIMAL; ANIMAL BEHAVIOR; BLOOD; C57BL MOUSE; FEMALE; IMMUNE SYSTEM; IMMUNOLOGY; MESENCEPHALON; METABOLISM; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; IMMUNE SYSTEM; LIPOPOLYSACCHARIDES; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SEROTONIN; SYNAPTIC TRANSMISSION;

EID: 84946202582     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.168     Document Type: Article

References (55)

1. Organization WH. Depression: A Global Public Health Concern, 2012.
2. Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006; 27: 24-31.
3. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008; 9: 46-56.
4. Zhu CB, Lindler KM, Owens AW, Daws LC, Blakely RD, Hewlett WA. Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacology 2010; 35: 2510-2520.
5. Wohleb ES, McKim DB, Sheridan JF, Godbout JP. Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-To-brain communication that influences mood and behavior. Front Neurosci 2014; 8: 447.
6. Baganz NL, Blakely RD. A dialogue between the immune system and brain, spoken in the language of serotonin. ACS Chem Neurosci 2013; 4: 48-63.
7. Gemma C, Ghezzi P, De Simoni MG. Activation of the hypothalamic serotoninergic system by central interleukin-1. Eur J Pharmacol 1991; 209: 139-140.
8. Shintani F, Kanba S, Nakaki T, Nibuya M, Kinoshita N, Suzuki E et al. Interleukin-1 beta augments release of norepinephrine, dopamine, and serotonin in the rat anterior hypothalamus. J Neurosci 1993; 13: 3574-3581.
9. Linthorst AC, Flachskamm C, Muller-Preuss P, Holsboer F, Reul JM. Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J Neurosci 1995; 15: 2920-2934.
10. Gemma C, Imeri L, de Simoni MG, Mancia M. Interleukin-1 induces changes in sleep, brain temperature, and serotonergic metabolism. Am J Physiol. 1997; 272(2 Pt 2): R601-R606.
11. Barkhudaryan N, Dunn AJ. Molecular mechanisms of actions of interleukin-6 on the brain, with special reference to serotonin and the hypothalamo-pituitaryadrenocortical axis. Neurochem Res 1999; 24: 1169-1180.
12. Wu Y, Shaghaghi EK, Jacquot C, Pallardy M, Gardier AM. Synergism between interleukin-6 and interleukin-1beta in hypothalamic serotonin release: a reverse in vivo microdialysis study in F344 rats. Eur Cytokine Netw 1999; 10: 57-64.
13. Yang ZJ, Blaha V, Meguid MM, Laviano A, Oler A, Zadak Z. Interleukin-1alpha injection into ventromedial hypothalamic nucleus of normal rats depresses food intake and increases release of dopamine and serotonin. Pharmacol Biochem Behav 1999; 62: 61-65.
14. Brebner K, Hayley S, Zacharko R, Merali Z, Anisman H. Synergistic effects of interleukin-1beta, interleukin-6, and tumor necrosis factor-Alpha: central monoamine, corticosterone, and behavioral variations. Neuropsychopharmacology 2000; 22: 566-580.
15. Zhang J, Terreni L, De Simoni MG, Dunn AJ. Peripheral interleukin-6 administration increases extracellular concentrations of serotonin and the evoked release of serotonin in the rat striatum. Neurochem Int 2001; 38: 303-308.
16. von Meyenburg C, Langhans W, Hrupka BJ. Evidence for a role of the 5-HT2C receptor in central lipopolysaccharide-, interleukin-1 beta-, and leptin-induced anorexia. Pharmacol Biochem Behav 2003; 74: 1025-1031.
17. Zhu CB, Hewlett WA, Feoktistov I, Biaggioni I, Blakely RD. 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.
18. Prasad HC, Zhu CB, McCauley JL, Samuvel DJ, Ramamoorthy S, Shelton RC et al. Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-Activated protein kinase. Proc Natl Acad Sci USA 2005; 102: 11545-11550.
19. Steiner JA, Carneiro AM, Blakely RD. Going with the flow: trafficking-dependent and -independent regulation of serotonin transport. Traffic 2008; 9: 1393-1402.
20. Zhu CB, Blakely RD, Hewlett WA. The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-Alpha activate serotonin transporters. Neuropsychopharmacology 2006; 31: 2121-2131.
21. Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008; 5: 10.
22. Aouadi M, Binetruy B, Caron L, Le Marchand-Brustel Y, Bost F. Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 2006; 88: 1091-1098.
23. Heinrichsdorff J, Luedde T, Perdiguero E, Nebreda AR, Pasparakis M. p38 alpha MAPK inhibits JNK activation and collaborates with IkappaB kinase 2 to prevent endotoxin-induced liver failure. EMBO Rep 2008; 9: 1048-1054.
24. Ventura JJ, Tenbaum S, Perdiguero E, Huth M, Guerra C, Barbacid M et al. p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat Genet 2007; 39: 750-758.
25. Scott MM, Wylie CJ, Lerch JK, Murphy R, Lobur K, Herlitze S et al. A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc Natl Acad Sci USA 2005; 102: 16472-16477.
26. Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N et al. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 2007; 27: 9817-9823.
27. Liu C, Maejima T, Wyler SC, Casadesus G, Herlitze S, Deneris ES. Pet-1 is required across different stages of life to regulate serotonergic function. Nat Neurosci 2010; 13: 1190-1198.
28. Zhu CB, Steiner JA, Munn JL, Daws LC, Hewlett WA, Blakely RD. Rapid stimulation of presynaptic serotonin transport by A(3) adenosine receptors. J Pharmacol Exp Ther 2007; 322: 332-340.
29. Schmittgen TD, Livak KJ. Analyzing real-Time PCR data by the comparative C (T) method. Nat Protoc 2008; 3: 1101-1108.
30. Thompson BJ, Jessen T, Henry LK, Field JR, Gamble KL, Gresch PJ et al. Transgenic elimination of high-Affinity antidepressant and cocaine sensitivity in the presynaptic serotonin transporter. Proc Natl Acad Sci USA 2011; 108: 3785-3790.
31. Veenstra-VanderWeele J, Muller CL, Iwamoto H, Sauer JE, Owens WA, Shah CR et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci USA 2012; 109: 5469-5474.
32. Steru L, Chermat R, Thierry B, Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 1985; 85: 367-370.
33. Samuvel DJ, Jayanthi LD, Bhat NR, Ramamoorthy S. A role for p38 mitogenactivated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J Neurosci 2005; 25: 29-41.
34. Bruchas MR, Schindler AG, Shankar H, Messinger DI, Miyatake M, Land BB et al. Selective p38alpha MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 2011; 71: 498-511.
35. Laye S, Parnet P, Goujon E, Dantzer R. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res Mol Brain Res 1994; 27: 157-162.
36. Cabrera R, Korte SM, Lentjes EG, Romijn F, Schonbaum E, De Nicola A et al. The amount of free corticosterone is increased during lipopolysaccharideinduced fever. Life Sci 2000; 66: 553-562.
37. Dantzer R. How do cytokines say hello to the brain? Neural versus humoral mediation. Eur Cytokine Netw 1994; 5: 271-273.
38. Dunn AJ. Nervous system-immune system interactions: an overview. J Recept Res 1988; 8: 589-607.
39. Weber A, Wasiliew P, Kracht M. Interleukin-1 (IL-1) pathway. Sci Signal 2010; 3: cm1.
40. Zhang J, Shen B, Lin A. Novel strategies for inhibition of the p38 MAPK pathway. Trends Pharmacol Sci 2007; 28: 286-295.
41. Zhu CB, Carneiro AM, Dostmann WR, Hewlett WA, Blakely RD. p38 MAPK activation elevates serotonin transport activity via a trafficking-independent, protein phosphatase 2 A-dependent process. J Biol Chem 2005; 280: 15649-15658.
42. Carneiro AM, Cook EH, Murphy DL, Blakely RD. Interactions between integrin alphaIIbbeta3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. J Clin Invest 2008; 118: 1544-1552.
43. Hollis JH, Evans AK, Bruce KP, Lightman SL, Lowry CA. Lipopolysaccharide has indomethacin-sensitive actions on Fos expression in topographically organized subpopulations of serotonergic neurons. Brain Behav Immun 2006; 20: 569-577.
44. Kopf BS, Langhans W, Geary N, Asarian L. Serotonin 2C receptor signaling in a diffuse neuronal network is necessary for LPS anorexia. Brain Res 2010; 1306: 77-84.
45. van Heesch F, Prins J, Konsman JP, Westphal KG, Olivier B, Kraneveld AD et al. Lipopolysaccharide-induced anhedonia is abolished in male serotonin transporter knockout rats: an intracranial self-stimulation study. Brain Behav Immun 2013; 29: 98-103.
46. van Heesch F, Prins J, Konsman JP, Korte-Bouws GA, Westphal KG, Rybka J et al. Lipopolysaccharide increases degradation of central monoamines: an in vivo microdialysis study in the nucleus accumbens and medial prefrontal cortex of mice. Eur J Pharmacol 2014; 725: 55-63.
47. Dunn AJ, Swiergiel AH. Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol Biochem Behav 2005; 81: 688-693.
48. Cryan JF, Mombereau C, Vassout A. The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 2005; 29: 571-625.
49. Detke MJ, Johnson J, Lucki I. Acute and chronic antidepressant drug treatment in the rat forced swimming test model of depression. Exp Clin Psychopharmacol 1997; 5: 107-112.
50. Swiergiel AH, Dunn AJ. Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol Biochem Behav 2007; 86: 651-659.
51. Lowry CA, Johnson PL, Hay-Schmidt A, Mikkelsen J, Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005; 8: 233-246.
52. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ et al. Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 2008; 1148: 86-94.
53. Ramamoorthy S, Giovanetti E, Qian Y, Blakely RD. Phosphorylation and regulation of antidepressant-sensitive serotonin transporters. J Biol Chem 1998; 273: 2458-2466.
54. Sorensen L, Stromgaard K, Kristensen AS. Characterization of intracellular regions in the human serotonin transporter for phosphorylation sites. ACS Chem Biol 2014; 9: 935-944.
55. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 3rd edn, Academic Press: New York, NY, USA, 2008.