AChE and RACK1 promote the anti-inflammatory properties of fluoxetine

Journal of Molecular Neuroscience

Volumn 53, Issue 3, 2014, Pages 306-315

  Waiskopf, Nir ^a   Ofek, Keren ^a   Gilboa Geffen, Adi ^a   Bekenstein, Uriya ^a   Bahat, Assaf ^a   Bennett, Estelle R ^a   Podoly, Erez ^a   Livnah, Oded ^a   Hartmann, Gunther ^b   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Acetylcholinesterase (AChE); Antidepressant; Cholinergic; Inflammation; Receptor for activated C kinase 1 (RACK1); Toll like receptor

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CITALOPRAM; DULOXETINE; ESCITALOPRAM; FLUOXETINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NEFAZODONE; PROTEIN KINASE B BETA; RECEPTOR FOR ACTIVATED C KINASE 1; SERTRALINE; TOLL LIKE RECEPTOR 4; TRAZODONE; TUMOR NECROSIS FACTOR ALPHA; VENLAFAXINE; ACHE PROTEIN, HUMAN; ANTIINFLAMMATORY AGENT; CELL SURFACE RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GNB2L1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN BINDING; PROTEIN KINASE C BETA; SEROTONIN UPTAKE INHIBITOR; TLR4 PROTEIN, HUMAN; TUMOR PROTEIN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE; MOLECULAR INTERACTION; MONONUCLEAR CELL; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR DOCKING; MOLECULAR GENETICS; MONOCYTE;

BACTERIA (MICROORGANISMS);

ACETYLCHOLINESTERASE; AMINO ACID SEQUENCE; ANTI-INFLAMMATORY AGENTS; BINDING SITES; FLUOXETINE; GPI-LINKED PROTEINS; GTP-BINDING PROTEINS; HUMANS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; MONOCYTES; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN KINASE C BETA; RECEPTORS, CELL SURFACE; SEROTONIN UPTAKE INHIBITORS; TOLL-LIKE RECEPTOR 4;

EID: 84905040142     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-013-0174-6     Document Type: Article

References (70)

1. Adams DR, Ron D, Kiely PA (2011) RACK1, a multifaceted scaffolding protein: structure and function. Cell Commun Signal 9:22
2. Akashi-Takamura S, Miyake K (2008) TLR accessory molecules. Curr Opin Immunol 20:420-425
3. Aksoy E, Amraoui Z, Goriely S, Goldman M, Willems F (2002) Critical role of protein kinase C epsilon for lipopolysaccharide-induced IL-12 synthesis in monocyte-derived dendritic cells. Eur J Immunol 32:3040-3049 (Pubitemid 35414861)
4. Bertrand C, Bonafos B, Tremblay M, Ferry A, Chatonnet A (2008) Effect of fluoxetine on neuromuscular function in acetylcholinesterase (AChE) knockout mice. Chem Biol Interact 175:113-114
5. Bird RJ, Baillie GS, Yarwood SJ (2010) Interaction with receptor for activated C-kinase 1 (RACK1) sensitizes the phosphodiesterase PDE4D5 towards hydrolysis of cAMP and activation by protein kinase C. Biochem J 432:207-216
6. Birikh KR, Sklan EH, Shoham S, Soreq H (2003) Interaction of "readthrough" acetylcholinesterase with RACK1 and PKCbeta II correlates with intensified fear-induced conflict behavior. Proc Natl Acad Sci U S A 100:283-288 (Pubitemid 36078066)
7. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW, Tracey KJ (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405:458-462 (Pubitemid 30367422)
8. Brandon NJ, Uren JM, Kittler JT, Wang H, Olsen R, Parker PJ, Moss SJ (1999) Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 19:9228-9234 (Pubitemid 30228075)
9. Brandon NJ, Jovanovic JN, Smart TG, Moss SJ (2002) Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors. J Neurosci 22:6353-6361 (Pubitemid 35386390)
10. Charles HC, Lazeyras F, Krishnan KR, Boyko OB, Payne M, Moore D (1994) Brain choline in depression: in vivo detection of potential pharmacodynamic effects of antidepressant therapy using hydrogen localized spectroscopy. Prog Neuropsychopharmacol Biol Psychiatry 18:1121-1127
11. Chen CC, Wang JK, Lin SB (1998) Antisense oligonucleotides targeting protein kinase C-alpha, -beta I, or -delta but not -eta inhibit lipopolysaccharide-induced nitric oxide synthase expression in RAW 264.7 macrophages: involvement of a nuclear factor kappa B-dependent mechanism. J Immunol 161:6206-6214
12. Chen YW, Rada PV, Butzler BP, Leibowitz SF, Hoebel BG (2012) Corticotropin-releasing factor in the nucleus accumbens shell induces swim depression, anxiety, and anhedonia along with changes in local dopamine/acetylcholine balance. Neuroscience 206:155-166
13. Coudronniere N, Villalba M, Englund N, Altman A (2000) NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc Natl Acad Sci U S A 97:3394-3399 (Pubitemid 30183313)
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 (Pubitemid 350295688)
15. Del Arco A, Segovia G, Garrido P, de Blas M, Mora F (2007) Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and workingmemory performance in rats. Behav Brain Res 176:267-273 (Pubitemid 44880088)
16. Dvir H, Harel M, Bon S, Liu WQ, Vidal M, Garbay C, Sussman JL, Massoulie J, Silman I (2004) The synaptic acetylcholinesterase tetramer assembles around a polyproline II helix. EMBO J 23:4394-4405 (Pubitemid 39601964)
17. Dvir H, Silman I, Harel M, Rosenberry TL, Sussman JL (2010) Acetylcholinesterase: from 3D structure to function. Chem Biol Interact 187:10-22
18. Fancy DA, Kodadek T (1999) Chemistry for the analysis of protein-protein interactions: rapid and efficient cross-linking triggered by long wavelength light. Proc Natl Acad Sci U S A 96:6020-6024 (Pubitemid 29256612)
19. Garate I, Garcia-Bueno B, Madrigal JL, Bravo L, Berrocoso E, Caso JR, Mico JA, Leza JC (2011) Origin and consequences of brain Toll-like receptor 4 pathway stimulation in an experimental model of depression. J Neuroinflammation 8:151
20. Gilboa-Geffen A, Hartmann G, Soreq H (2012) Stressing hematopoiesis and immunity: an acetylcholinesterase window into nervous and immune system interactions. Front Mol Neurosci 5:30
21. Grisaru D, Pick M, Perry C, Sklan EH, Almog R, Goldberg I, Naparstek E, Lessing JB, Soreq H, Deutsch V (2006) Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. J Immunol 176:27-35 (Pubitemid 43023245)
22. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723 (Pubitemid 28059943)
23. He DY, Neasta J, Ron D (2010) Epigenetic regulation of BDNF expression via the scaffolding protein RACK1. J Biol Chem 285:19043-19050
24. Hutchinson MR, Loram LC, Zhang Y, Shridhar M, Rezvani N, Berkelhammer D, Phipps S, Foster PS, Landgraf K, Falke JJ et al (2010) Evidence that tricyclic small molecules may possess toll-like receptor and myeloid differentiation protein 2 activity. Neuroscience 168:551-563
25. Irwin JJ, Sterling T, Mysinger MM, Bolstad ES, Coleman RG (2012) ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52:1757-1768
26. Iwamoto T, Hagiwara M, Hidaka H, Isomura T, Kioussis D, Nakashima I (1992) Accelerated proliferation and interleukin-2 production of thymocytes by stimulation of soluble anti-CD3 monoclonal antibody in transgenic mice carrying a rabbit protein kinase C alpha. J Biol Chem 267:18644-18648
27. Kagan JC, Medzhitov R (2006) Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125:943-955 (Pubitemid 43795199)
28. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373-384
29. Koran LM, Cain JW, Dominguez RA, Rush AJ, Thiemann S (1996) Are fluoxetine plasma levels related to outcome in obsessive-compulsive disorder? Am J Psychiatry 153:1450-1454 (Pubitemid 26365460)
30. Leitges M, Schmedt C, Guinamard R, Davoust J, Schaal S, Stabel S, Tarakhovsky A (1996) Immunodeficiency in protein kinase cbeta-deficient mice. Science 273:788-791 (Pubitemid 26271522)
31. Leonard BE (2010) The concept of depression as a dysfunction of the immune system. Curr Immunol Rev 6:205-212
32. Leppanen T, Jalonen U, Kankaanranta H, Tuominen R, Moilanen E (2008) Inhibition of protein kinase C beta II downregulates tristetraprolin expression in activated macrophages. Inflamm Res 57:230-240 (Pubitemid 351929677)
33. Liu D, Wang Z, Liu S, Wang F, Zhao S, Hao A (2011) Anti-inflammatory effects of fluoxetine in lipopolysaccharide(LPS)-stimulated microglial cells. Neuropharmacology 61:592-599
34. Loegering DJ, Lennartz MR (2011) Protein kinase C and toll-like receptor signaling. Enzym Res 2011:537821
35. Maggi L, Palma E, Miledi R, Eusebi F (1998) Effects of fluoxetine on wild and mutant neuronal alpha 7 nicotinic receptors. Mol Psychiatry 3:350-355 (Pubitemid 28379921)
36. Mineur YS, Obayemi A, Wigestrand MB, Fote GM, Calarco CA, Li AM, Picciotto MR (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci U S A 110:3573-3578
37. Mochly-Rosen D, Khaner H, Lopez J, Smith BL (1991) Intracellular receptors for activated protein kinase C. Identification of a binding site for the enzyme. J Biol Chem 266:14866-14868 (Pubitemid 21907586)
38. Nilsson J, Sengupta J, Frank J, Nissen P (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 5:1137-1141 (Pubitemid 40103606)
39. O'Brien SM, Scully P, Fitzgerald P, Scott LV, Dinan TG (2007) Plasma cytokine profiles in depressed patients who fail to respond to selective serotonin reuptake inhibitor therapy. J Psychiatr Res 41:326-331 (Pubitemid 44854992)
40. Ofek K, Schoknecht K, Melamed-Book N, Heinemann U, Friedman A, Soreq H (2012) Fluoxetine induces vasodilatation of cerebral arterioles by co-modulating NO/muscarinic signalling. J Cell Mol Med 16:2736-2744
41. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458:1191-1195
42. Perry C, Pick M, Podoly E, Gilboa-Geffen A, Zimmerman G, Sklan EH, Ben-Shaul Y, Diamant S, Soreq H (2007) Acetylcholinesterase/C terminal binding protein interactions modify Ikaros functions, causing T lymphopenia. Leukemia 21:1472-1480 (Pubitemid 46965289)
43. Pick M, Perry C, Lapidot T, Guimaraes-Sternberg C, Naparstek E, Deutsch V, Soreq H (2006) Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood 107:3397-3406
44. Pierce BG, Hourai Y, Weng Z (2011) Accelerating protein docking in ZDOCK using an advanced 3D convolution library. PLoS One 6:e24657
45. Prado VF, Roy A, Kolisnyk B, Gros R, Prado MA (2013) Regulation of cholinergic activity by the vesicular acetylcholine transporter. Biochem J 450:265-274
46. Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc Natl Acad Sci U S A 91:839-843 (Pubitemid 24048462)
47. Ron D, Jiang Z, Yao L, Vagts A, Diamond I, Gordon A (1999) Coordinated movement of RACK1 with activated betaIIPKC. J Biol Chem 274:27039-27046
48. Rosas-Ballina M, Tracey KJ (2009) The neurology of the immune system: neural reflexes regulate immunity. Neuron 64:28-32
49. Ruiz Carrillo D, Chandrasekaran R, Nilsson M, Cornvik T, Liew CW, Tan SM, Lescar J (2012) Structure of human Rack1 protein at a resolution of 2.45 A. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:867-872
50. Russo P, Taly A (2012) alpha7-Nicotinic acetylcholine receptors: an old actor for new different roles. Curr Drug Targets 13:574-578
51. Sacre S, Medghalchi M, Gregory B, Brennan F, Williams R (2010) Fluoxetine and citalopram exhibit potent antiinflammatory activity in human and murine models of rheumatoid arthritis and inhibit toll-like receptors. Arthritis Rheum 62:683-693
52. Saijo K, Schmedt C, Su IH, Karasuyama H, Lowell CA, Reth M, Adachi T, Patke A, Santana A, Tarakhovsky A (2003) Essential role of Src-family protein tyrosine kinases in NF-kappaB activation during B cell development. Nat Immunol 4:274-279 (Pubitemid 36322138)
53. Saito N, Kikkawa U, Nishizuka Y (2002) The family of protein kinase C and membrane lipid mediators. J Diabetes Complications 16:4-8 (Pubitemid 34168492)
54. Sands WA, Bulut V, Severn A, Xu D, Liew FY (1994) Inhibition of nitric oxide synthesis by interleukin-4 may involve inhibiting the activation of protein kinase C epsilon. Eur J Immunol 24:2345-2350
55. Sanner MF (1999) Python: a programming language for software integration and development. J Mol Graph Model 17:57-61
56. Santaguida PL, MacQueen G, Keshavarz H, Levine M, Beyene J, Raina P (2012) Treatment for depression after unsatisfactory response to SSRIs. Agency for Healthcare Research and Quality, Rockville
57. Shaked I, Meerson A, Wolf Y, Avni R, Greenberg D, Gilboa-Geffen A, Soreq H (2009) MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 31:965-973
58. Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K, Kimoto M (1999) MD-2, amolecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 189:1777-1782 (Pubitemid 29272694)
59. Sklan EH, Podoly E, Soreq H (2006) RACK1 has the nerve to act: structure meets function in the nervous system. Prog Neurobiol 78:117-134 (Pubitemid 43290718)
60. Sluzewska A, Rybakowski JK, Laciak M, Mackiewicz A, Sobieska M, Wiktorowicz K (1995) Interleukin-6 serum levels in depressed patients before and after treatment with fluoxetine. Ann N Y Acad Sci 762:474-476
61. Soreq H, Seidman S (2001) Acetylcholinesterase-new roles for an old actor. Nat Rev Neurosci 2:294-302
62. Stebbins EG, Mochly-Rosen D (2001) Binding specificity for RACK1 resides in the V5 region of beta II protein kinase C. J Biol Chem 276:29644-29650
63. Steingard RJ, Yurgelun-Todd DA, Hennen J, Moore JC, Moore CM, Vakili K, Young AD, Katic A, Beardslee WR, Renshaw PF (2000) Increased orbitofrontal cortex levels of choline in depressed adolescents as detected by in vivo proton magnetic resonance spectroscopy. Biol Psychiatry 48:1053-1061
64. Tarsy D, Leopold N, Sax DS (1972) Cholinergic-adrenergic hypothesis of mania and depression. Lancet 2:1153
65. Thornton C, Tang KC, Phamluong K, Luong K, Vagts A, Nikanjam D, Yaka R, Ron D (2004) Spatial and temporal regulation of RACK1 function and N-methyl-D-aspartate receptor activity through WD40 motif-mediated dimerization. J Biol Chem 279:31357-31364 (Pubitemid 39037802)
66. Tracey KJ (2002) The inflammatory reflex. Nature 420:853-859
67. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455-461
68. Valledor AF, Xaus J, Comalada M, Soler C, Celada A (2000) Protein kinase C epsilon is required for the induction of mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J Immunol 164:29-37 (Pubitemid 30012968)
69. Weeber EJ, Atkins CM, Selcher JC, Varga AW, Mirnikjoo B, Paylor R, Leitges M, Sweatt JD (2000) A role for the beta isoform of protein kinase C in fear conditioning. J Neurosci 20:5906-5914 (Pubitemid 30658381)
70. Zimmerman G, Shaltiel G, Barbash S, Cohen J, Gasho CJ, Shenhar-Tsarfaty S, Shalev H, Berliner SA, Shelef I, Shoham S et al (2012) Post-traumatic anxiety associates with failure of the innate immune receptor TLR9 to evade the pro-inflammatory NFkappaB pathway. Transl Psychiatry 2:e78