Interleukin-6 attenuates serotonin 2A receptor signaling by activating the JAK-STAT pathway

Molecular Pharmacology

Volumn 87, Issue 3, 2015, Pages 492-500

  Donegan, Jennifer J ^a   Patton, Michael S ^a   Chavera, Teresa S ^a   Berg, Kelly A ^a   Morilak, David A ^a   Girotti, Milena ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; BRADYKININ B2 RECEPTOR; G PROTEIN COUPLED RECEPTOR; INTERLEUKIN 6; JANUS KINASE; JANUS KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN INHIBITOR OF ACTIVATED STAT; RNA; SEROTONIN 2A RECEPTOR; STAT PROTEIN; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; GENE SILENCING; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; ENZYME ACTIVATION; MALE; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL LINE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; INTERLEUKIN-6; JANUS KINASES; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2A; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84921473245     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.096289     Document Type: Article

References (39)

1. Baier PC, May U, Scheller J, Rose-John S, and Schiffelholz T (2009) Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice. Behav Brain Res 200:192-196.
2. Banes AKL, Shaw SM, Tawfik A, Patel BP, Ogbi S, Fulton D, and Marrero MB (2005) Activation of the JAK/STAT pathway in vascular smooth muscle by serotonin. Am J Physiol Cell Physiol 288:C805-C812.
3. Beck AT (2008) The evolution of the cognitive model of depression and its neurobiological correlates. Am J Psychiatry 165:969-977.
4. Berg KA, Clarke WP, Chen Y, Ebersole BJ, McKay RD, and Maayani S (1994) 5-Hydroxytryptamine type 2A receptors regulate cyclic AMP accumulation in a neuronal cell line by protein kinase C-dependent and calcium/calmodulin-dependent mechanisms. Mol Pharmacol 45:826-836.
5. Berg KA, Maayani S, Goldfarb J, Scaramellini C, Leff P, and Clarke WP (1998) Effector pathway-dependent relative efficacy at serotonin type 2A and 2C receptors: evidence for agonist-directed trafficking of receptor stimulus. Mol Pharmacol 54:94-104.
6. Carr GV and Lucki I (2011) The role of serotonin receptor subtypes in treating depression: a review of animal studies. Psychopharmacology (Berl) 213:265-287.
7. de Almeida J and Mengod G (2007) Quantitative analysis of glutamatergic and GABAergic neurons expressing 5-HT(2A) receptors in human and monkey prefrontal cortex. J Neurochem 103:475-486.
8. De-Fraja C, Conti L, Magrassi L, Govoni S, and Cattaneo E (1998) Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J Neurosci Res 54:320-330.
9. Donegan JJ, Girotti M, Weinberg MS, and Morilak DA (2014) A novel role for brain interleukin-6: facilitation of cognitive flexibility in rat orbitofrontal cortex. J Neurosci 34:953-962.
10. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, and Lanctôt KL (2010) A meta-analysis of cytokines in major depression. Biol Psychiatry 67:446-457.
11. Dugan LL, Ali SS, Shekhtman G, Roberts AJ, Lucero J, Quick KL, and Behrens MM (2009) IL-6 mediated degeneration of forebrain GABAergic interneurons and cognitive impairment in aged mice through activation of neuronal NADPH oxidase. PLoS ONE 4:e5518.
12. Fletcher PJ, Tampakeras M, Sinyard J, and Higgins GA (2007) Opposing effects of 5-HT(2A) and 5-HT(2C) receptor antagonists in the rat and mouse on premature responding in the five-choice serial reaction time test. Psychopharmacology (Berl) 195:223-234.
13. Furr A, Lapiz-Bluhm MD, and Morilak DA (2012) 5-HT2A receptors in the orbitofrontal cortex facilitate reversal learning and contribute to the beneficial cognitive effects of chronic citalopram treatment in rats. Int J Neuropsychopharmacol 15:1295-1305.
14. Garcia-Oscos F, Salgado H, Hall S, Thomas F, Farmer GE, Bermeo J, Galindo LC, Ramirez RD, D'Mello S, and Rose-John S et al. (2012) The stress-induced cytokine interleukin-6 decreases the inhibition/excitation ratio in the rat temporal cortex via trans-signaling. Biol Psychiatry 71:574-582.
15. Gellman RL and Aghajanian GK (1994) Serotonin2 receptor-mediated excitation of interneurons in piriform cortex: antagonism by atypical antipsychotic drugs. Neuroscience 58 :515-525.
16. Gimeno D, Kivimäki M, Brunner EJ, Elovainio M, De Vogli R, Steptoe A, Kumari M, Lowe GDO, Rumley A, and Marmot MG et al. (2009) Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychol Med 39:413-423.
17. Gray JA and Roth BL (2001) Paradoxical trafficking and regulation of 5-HT(2A) receptors by agonists and antagonists. Brain Res Bull 56:441-451.
18. Guillet-Deniau I, Burnol A-F, and Girard J (1997) Identification and localization of a skeletal muscle secrotonin 5-HT2A receptor coupled to the Jak/STAT pathway. J Biol Chem 272:14825-14829.
19. Gurevich EV and Joyce JN (1997) Alterations in the cortical serotonergic system in schizophrenia: a postmortem study. Biol Psychiatry 42:529-545.
20. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, and Schaper F (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374:1-20.
21. Kehagia AA, Murray GK, and Robbins TW (2010) Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr Opin Neurobiol 20: 199-204.
22. Leysen JE (2004) 5-HT2 receptors. Curr Drug Targets CNS Neurol Disord 3:11-26.
23. Matsuda S, Wen T-C, Morita F, Otsuka H, Igase K, Yoshimura H, and Sakanaka M (1996) Interleukin-6 prevents ischemia-induced learning disability and neuronal and synaptic loss in gerbils. Neurosci Lett 204: 109-112.
24. Meltzer HY (2012) Serotonergic mechanisms as targets for existing and novel antipsychotics, in Current Antipsychotics (Gross G and Geyer MA eds) pp 87-124, Springer, Berlin.
25. Nichols DE and Nichols CD (2008) Serotonin receptors. Chem Rev 108:1614-1641.
26. Pompeiano M, Palacios JM, and Mengod G (1994) Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Mol Brain Res 23 : 163-178.
27. Puig MV, Celada P, Díaz-Mataix L, and Artigas F (2003) In vivo modulation of the activity of pyramidal neurons in the rat medial prefrontal cortex by 5-HT2A receptors: relationship to thalamocortical afferents. Cereb Cortex 13:870-882.
28. Remijnse PL, Nielen MMA, van Balkom AJLM, Cath DC, van Oppen P, Uylings HBM, and Veltman DJ (2006) Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder. Arch Gen Psychiatry 63:1225-1236.
29. Santana N, Bortolozzi A, Serrats J, Mengod G, and Artigas F (2004) Expression of serotonin1A and serotonin2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 14:1100-1109.
30. Shelton RC, Sanders-Bush E, Manier DH, and Lewis DA (2009) Elevated 5-HT 2A receptors in postmortem prefrontal cortex in major depression is associated with reduced activity of protein kinase A. Neuroscience 158:1406-1415.
31. Singh RK, Dai Y, Staudinger JL, and Muma NA (2009) Activation of the JAK-STAT pathway is necessary for desensitization of 5-HT2A receptor-stimulated phospholipase C signalling by olanzapine, clozapine and MDL 100907. Int J Neuropsychopharmacol 12:651-665.
32. Singh RK, Jia C, Garcia F, Carrasco GA, Battaglia G, and Muma NA (2010) Activation of the JAK-STAT pathway by olanzapine is necessary for desensitization of serotonin2A receptor-stimulated phospholipase C signaling in rat frontal cortex but not serotonin2A receptor-stimulated hormone release. J Psychopharmacol 24:1079-1088.
33. Singh RK, Shi J, Zemaitaitis BW, and Muma NA (2007) Olanzapine increases RGS7 protein expression via stimulation of the Janus tyrosine kinase-signal transducer and activator of transcription signaling cascade. J Pharmacol Exp Ther 322:133-140.
34. Sparkman NL, Buchanan JB, Heyen JRR, Chen J, Beverly JL, and Johnson RW (2006) Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J Neurosci 26:10709-10716.
35. Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell JE, Jr, and Yancopoulos GD (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267:1349-1353.
36. Urban JD, Clarke WP, von Zastrow M, Nichols DE, Kobilka B, Weinstein H, Javitch JA, Roth BL, Christopoulos A, and Sexton PM et al. (2007) Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320:1-13.
37. Willins DL, Deutch AY, and Roth BL (1997) Serotonin 5-HT2A receptors are expressed on pyramidal cells and interneurons in the rat cortex. Synapse 27:79-82.
38. Winstanley CA, Chudasama Y, Dalley JW, Theobald DE, Glennon JC, and Robbins TW (2003) Intra-prefrontal 8-OH-DPAT and M100907 improve visuospatial attention and decrease impulsivity on the five-choice serial reaction time task in rats. Psychopharmacology (Berl) 167:304-314.
39. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, and Hoshijima M et al. (2003) IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 4:551-556.