Interleukin 18 activates MAPKs and STAT3 but not NF-κB in hippocampal HT-22 cells

Brain, Behavior, and Immunity

Volumn 40, Issue , 2014, Pages 85-94

  Alboni, Silvia ^a   Montanari, Claudia ^a   Benatti, Cristina ^a   Sanchez Alavez, Manuel ^b   Rigillo, Giovanna ^a   Blom, Joan M C ^a   Brunello, Nicoletta ^a   Conti, Bruno ^b   Pariante, M Carmine ^c   Tascedda, Fabio ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Brain; Hippocampus; HT 22; IL 18; IL 18R ; IL 18R ; Isoforms; NF B; Signaling; STAT 3

Indexed keywords

ALPHA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 18 RECEPTOR BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; STAT3 PROTEIN; INTERLEUKIN 18 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; RECOMBINANT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HIPPOCAMPUS; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; METABOLISM;

ANIMALS; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; INTERLEUKIN-18; MALE; MICE; MICE, INBRED C57BL; NEURONS; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, INTERLEUKIN-18; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84904281158     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.02.015     Document Type: Article

References (80)

1. Abdul-Careem M.F., Hunter B.D., Sarson A.J., Mayameei A., Zhou H., Sharif S. Marek's disease virus-induced transient paralysis is associated with cytokine gene expression in the nervous system. Vir. Immunol. 2006, 19:167-176.
2. Alboni S., Cervia D., Ross B., Montanari C., Gonzalez A.S., Sanchez-Alavez M., Marcondes M.C., De Vries D., Sugama S., Brunello N., Blom J., Tascedda F., Conti B. Mapping of the full length and the truncated interleukin-18 receptor alpha in the mouse brain. J. Neuroimmunol. 2009, 214:43-54.
3. Alboni S., Cervia D., Sugama S., Conti B. Interleukin 18 in the CNS. J. Neuroinflamm. 2010, 7:9. 10.1186/1742-2094-7-9.
4. Alboni S., Montanari C., Benatti C., Blom J.M., Simone M.L., Brunello N., Caggia F., Guidotti G., Marcondes M.C., Sanchez-Alavez M., Conti B., Tascedda F. Constitutive and LPS-regulated expression of interleukin-18 receptor beta variants in the mouse brain. Brain Behav. Immun. 2011, 25:483-493.
5. Alboni S., Tascedda F., Corsini D., Benatti C., Caggia F., Capone G., Barden N., Blom J.M., Brunello N. Stress induces altered CRE/CREB pathway activity and BDNF expression in the hippocampus of glucocorticoid receptor-impaired mice. Neuropharmacology 2011, 60:1337-1346.
6. Alboni S., Gibellini L., Montanari C., Benatti C., Benatti S., Tascedda F., Brunello N., Cossarizza A., Pariante C.M. N-acetyl-cysteine prevents toxic oxidative effects induced by IFN-α in human neurons. Int. J. Neuropsychopharmacol. 2013, 16:1-17.
7. Andoh T., Kishi H., Motoki K., Nakanishi K., Kuraishi Y., Muraguchi A. Protective effect of IL-18 on kainate- and IL-1 beta-induced cerebellar ataxia in mice. J. Immunol. 2008, 180:2322-2328.
8. Andre R., Wheeler R.D., Collins P.D., Luheshi G.N., Pickering-Brown S., Kimber I., Rothwell N.J., Pinteaux E. Identification of a truncated IL-18R beta mRNA: a putative regulator of IL-18 expressed in rat brain. J. Neuroimmunol. 2003, 145:40-45.
9. Arend W.P., Palmer G., Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 2008, 223:20-38.
10. Benatti C., Alboni S., Montanari C., Caggia F., Tascedda F., Brunello N., Blom J.M. Central effects of a local inflammation in three commonly used mouse strains with a different anxious phenotype. Behav. Brain Res. 2011, 224:23-34.
11. Blom J.M., Benatti C., Alboni S., Capone G., Ferraguti C., Brunello N., Tascedda F. Early postnatal chronic inflammation produces long-term changes in pain behavior and N-methyl-D-aspartate receptor subtype gene expression in the central nervous system of adult mice. J Neurosci Res 2006, 84:1789-1798.
12. Bossù P., Ciaramella A., Salani F., Bizzoni F., Varsi E., Di Iulio F., Giubilei F., Gianni W., Trequattrini A., Moro M.L., Bernardini S., Caltagirone C., Spalletta G. Interleukin-18 produced by peripheral blood cells is increased in Alzheimer's disease and correlates with cognitive impairment. Brain Behav. Immun. 2008, 22:487-492.
13. Buss H., Dörrie A., Schmitz M.L., Hoffmann E., Resch K., Kracht M. Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 2004, 279:55633-55643.
14. Cattaneo E., Conti L., De-Fraja C. Signalling through the JAK-STAT pathway in the developing brain. Trends Neurosci. 1999, 22:365-369.
15. Cheng X., Jin G., Zhang X., Tian M., Zou L. Stage-dependent STAT3 activation is involved in the differentiation of rat hippocampus neural stem cells. Neurosci. Lett. 2011, 493:18-23.
16. Chung J., Uchida E., Grammer T.C., Blenis J. STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell. Biol. 1997, 17:6508-6516.
17. Cumiskey D., Curran B.P., Herron C.E., O'Connor J.J. A role for inflammatory mediators in the IL-18 mediated attenuation of LTP in the rat dentate gyrus. Neuropharmacology 2007, 52:1616-1623.
18. Curran B., O'Connor J.J. The pro-inflammatory cytokine interleukin-18 impairs long-term potentiation and NMDA receptor-mediated transmission in the rat hippocampus in vitro. Neuroscience 2001, 108:83-90.
19. Davis J.B., Maher P. Protein kinase C activation inhibits glutamate-induced cytotoxicity in a neuronal cell line. Brain Res 1994, 652:169-173.
20. De-Fraja C., Conti L., Magrassi L., Govoni S., Cattaneo E. Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J. Neurosci. Res. 1998, 54:320-330.
21. Decker T., Kovarik P. Serine phosphorylation of STATs. Oncogene 2000, 19:2628-2637.
22. del Rey A., Balschun D., Wetzel W., Randolf A., Besedovsky H.O. A cytokine network involving brain-borne IL-1β, IL-1ra, IL-18, IL-6, and TNFα operates during long-term potentiation and learning. Brain Behav. Immun. 2013, 2013(33):15-23.
23. Fiszer D., Rozwadowska N., Rychlewski L., Kosicki W., Kurpisz M. Identification of IL-18RAP mRNA truncated splice variants in human testis and the other human tissues. Cytokine 2007, 39:178-183.
24. Fortin C.F., Ear T., McDonald P.P. Autocrine role of endogenous interleukin-18 on inflammatory cytokine generation by human neutrophils. FASEB J. 2009, 23:194-203.
25. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2001, Academic, San Diego, CA. 2nd ed.
26. Haastrup E., Bukh J.D., Bock C., Vinberg M., Thørner L.W., Hansen T., Werge T., Kessing L.V., Ullum H. Promoter variants in IL18 are associated with onset of depression in patients previously exposed to stressful-life events. J. Affect. Disord. 2012, 136:134-138.
27. Han K.J., Yang Y., Xu L.G., Shu H.B. Analysis of a TIR-less splice variant of TRIF reveals an unexpected mechanism of TLR3-mediated signaling. J. Biol. Chem. 2010, 285:12543-12550.
28. Huang W.X., Huang P., Hillert J. Increased expression of caspase-1 and interleukin-18 in peripheral blood mononuclear cells in patients with multiple sclerosis. Mult. Scler. 2004, 10:482-487.
29. Hosoi T., Okuma Y., Kawagishi T., Qi X., Matsuda T., Nomura Y. Bacterial endotoxin induces STAT3 activation in the mouse brain. Brain Res. 2004, 1023:48-53.
30. Hu F., Pace T.W., Miller A.H. Interferon-alpha inhibits glucocorticoid receptor-mediated gene transcription via STAT5 activation in mouse HT-22 cells. Brain Behav. Immun. 2009, 23:455-463.
31. Iannello A., Samarani S., Debbeche O., Tremblay C., Toma E., Boulassel M.R., Routy J.P., Ahmad A. Role of interleukin-18 in the development and pathogenesis of AIDS. AIDS Rev. 2009, 11:115-125.
32. Jung H.K., Ryu H.J., Kim M.J., Kim W.I., Choi H.K., Choi H.C., Song H.K., Jo S.M., Kang T.C. Interleukin-18 attenuates disruption of brain-blood barrier induced by status epilepticus within the rat piriform cortex in interferon-γ independent pathway. Brain Res. 2012, 1447:126-134.
33. Kalina U., Kauschat D., Koyama N., Nuernberger H., Ballas K., Koschmieder S., Bug G., Hofmann W.K., Hoelzer D., Ottmann O.G. IL-18 activates STAT3 in the natural killer cell line 92, augments cytotoxic activity, and mediates IFNgamma production by the stress kinase p38 and by the extracellular regulated kinases p44erk-1 and p42erk-21. J. Immunol. 2000, 165:1307-1313.
34. Kim Y.M., Kang H.S., Paik S.G., Pyun K.H., Anderson K.L., Torbett B.E., Choi I. Roles of IFN consensus sequence binding protein and PU.1 in regulating IL-18 gene expression. J. Immunol. 1999, 163:2000-2007.
35. Kokai M., Kashiwamura S., Okamura H., Ohara K., Morita Y. Plasma interleukin-18 levels in patients with psychiatric disorders. J. Immunother. 2002, 25(Suppl. 1):S68-S71.
36. Kroeger K.M., Sullivan B.M., Locksley R.M. IL-18 and IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38alpha-dependent pathway. J. Leukoc. Biol. 2009, 86:769-778.
37. Kroes R.A., Panksepp J., Burgdorf J., Otto N.J., Moskal J.R. Modeling depression: social dominance-submission gene expression patterns in rat neocortex. Neuroscience 2006, 137:37-49.
38. Kumar R.A., Cann C., Hall J.E., Sudheer P.S., Wilkes A.R. Predictive value of IL-18 and SC5b-9 for neurocognitive dysfunction after cardiopulmonary bypass. Br. J. Anaesth. 2007, 98:317-322.
39. Lappas M., Permezel M., Georgiou H.M., Rice G.E. Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro. Biol. Reprod. 2002, 67:668-673.
40. Lee J.K., Kim S.H., Lewis E.C., Azam T., Reznikov L.L., Dinarello C.A. Differences in signaling pathways by IL-1beta and IL-18. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8815-8820.
41. Li Q., Verma I.M. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2002, 2:725-734.
42. Liu Y.P., Lin H.I., Tzeng S.F. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res. 2005, 1054:152-158.
43. Losy J., Niezgoda A. IL-18 in patients with multiple sclerosis. Acta Neurol. Scand. 2001, 104:171-173.
44. Lu L.X., Guo S.Q., Chen W., Li Q., Cheng J., Guo J.H. Effect of clozapine and risperidone on serum cytokine levels in patients with first-episode paranoid schizophrenia. Di Yi Jun Yi Da Xue Xue Bao 2004, 24:1251-1254.
45. Matsumoto S., Tsuji-Takayama K., Aizawa Y., Koide K., Takeuchi M., Ohta T., Kurimoto M. Interleukin-18 activates NF-kappaB in murine T helper type 1 cells. Biochem. Biophys. Res. Commun. 1997, 234:454-457.
46. Morel J.C., Park C.C., Woods J.M., Koch A.E. A novel role for interleukin-18 in adhesion molecule induction through NF kappa B and phosphatidylinositol (PI) 3-kinase-dependent signal transduction pathways. J. Biol. Chem. 2001, 276:37069-37075.
47. Morel J.C., Park C.C., Zhu K., Kumar P., Ruth J.H., Koch A.E. Signal transduction pathways involved in rheumatoid arthritis synovial fibroblast interleukin-18-induced vascular cell adhesion molecule-1 expression. J. Biol. Chem. 2002, 277:34679-34691.
48. Müller S., Chakrapani B.P., Schwegler H., Hofmann H.D., Kirsch M. Neurogenesis in the dentate gyrus depends on ciliary neurotrophic factor and signal transducer and activator of transcription 3 signaling. Stem Cells 2009, 27:431-441.
49. Murase S., Kim E., Lin L., Hoffman D.A., McKay R.D. Loss of signal transducer and activator of transcription 3 (STAT3) signaling during elevated activity causes vulnerability in hippocampal neurons. J. Neurosci. 2012, 32:15511-15520.
50. Murata S., Usuda N., Okano A., Kobayashi S., Suzuki T. Occurrence of a transcription factor, signal transducer and activators of transcription 3 (Stat3), in the postsynaptic density of the rat brain. Brain Res. Mol. Brain Res. 2000, 78:80-90.
51. Nakahira M., Ahn H.J., Park W.R., Gao P., Tomura M., Park C.S., Hamaoka T., Ohta T., Kurimoto M., Fujiwara H. Synergy of IL-12 and IL-18 for IFN-gamma gene expression: IL-12-induced STAT4 contributes to IFN-gamma promoter activation by up-regulating the binding activity of IL-18-induced activator protein 1. J. Immunol. 2002, 168:1146-1153.
52. Nakanishi K., Yoshimoto T., Tsutsui H., Okamura H. Interleukin-18 is a unique cytokine that stimulates both Th1 and Th2 responses depending on its cytokine milieu. Cytok. Growth Factor Rev. 2001, 12:53-72.
53. Natoli G., Saccani S., Bosisio D., Marazzi I. Interactions of NF-kappaB with chromatin: the art of being at the right place at the right time. Nat. Immunol. 2005, 6:439-445.
54. Ng D.C., Long C.S., Bogoyevitch M.A. A role for the extracellular signal-regulated kinase and p38 mitogen-activated protein kinases in interleukin-1 beta-stimulated delayed signal tranducer and activator of transcription 3 activation, atrial natriuretic factor expression, and cardiac myocyte morphology. J. Biol. Chem. 2001, 276:29490-29498.
55. Nicolas C.S., Amici M., Bortolotto Z.A., Doherty A., Csaba Z., Fafouri A., Dournaud P., Gressens P., Collingridge G.L., Peineau S. The role of JAK-STAT signaling within the CNS. JAKSTAT 2013, 2:e22925.
56. Novick D., Kim S.H., Fantuzzi G., Reznikov L.L., Dinarello C.A., Rubinstein M. Interleukin-18 binding protein: a novel modulator of the Th1 cytokine response. Immunity 1999, 10:127-136.
57. Olee T., Hashimoto S., Quach J., Lotz M. IL-18 is produced by articular chondrocytes and induces proinflammatory and catabolic responses. J. Immunol. 1999, 162:1096-1100.
58. Oztürk C., Ozge A., Yalin O.O., Yilmaz I.A., Delialioglu N., Yildiz C., Tesdelen B., Kudiaki C. The diagnostic role of serum inflammatory and soluble proteins on dementia subtypes: correlation with cognitive and functional decline. Behav. Neurol. 2007, 2007(18):207-215.
59. Pace T.W., Hu F., Miller A.H. Activation of cAMP-protein kinase A abrogates STAT5-mediated inhibition of glucocorticoid receptor signaling by interferon-alpha. Brain Behav. Immun. 2011, 25:1716-1724.
60. Rankin J.S., Zalcman S.S., Zhu Y., Siegel A. Short- and long-term effects of interleukin-2 treatment on the sensitivity of periadolescent female mice to interleukin-2 and dopamine uptake inhibitor. PLoS One 2013, 8:e64473.
61. Reddy V.S., Prabhu S.D., Mummidi S., Valente A.J., Venkatesan B., Shanmugam P., Delafontaine P., Chandrasekar B. Interleukin-18 induces EMMPRIN expression in primary cardiomyocytes via JNK/Sp1 signaling and MMP-9 in part via EMMPRIN and through AP-1 and NF-kappaB activation. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H1242-H1254.
62. Ryu H.J., Kim J.E., Kim M.J., Kwon H.J., Suh S.W., Song H.K., Kang T.C. The protective effects of interleukin-18 and interferon-γ on neuronal damages in the rat hippocampus following status epilepticus. Neuroscience 2010, 170:711-721.
63. Sahar S., Dwarakanath R.S., Reddy M.A., Lanting L., Todorov I., Natarajan R. Angiotensin II enhances interleukin-18 mediated inflammatory gene expression in vascular smooth muscle cells: a novel cross-talk in the pathogenesis of atherosclerosis. Circ. Res. 2005, 96:1064-1071.
64. Satoh Y., Endo S., Ikeda T., Yamada K., Ito M., Kuroki M., Hiramoto T., Imamura O., Kobayashi Y., Watanabe Y., Itohara S., Takishima K. Extracellular signal-regulated kinase 2 (ERK2) knockdown mice show deficits in long-term memory; ERK2 has a specific function in learning and memory. J. Neurosci. 2007, 27:10765-10776.
65. Schmidt A.J., Krieg J.C., Vedder H. Interleukin-6 induces glutathione in hippocampal cells. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:321-326.
66. Sergi B., Penttila I. Interleukin 18 receptor. J. Biol. Regul. Homeost. Agents 2004, 18:55-61.
67. Shelton R.C., Claiborne J., Sidoryk-Wegrzynowicz M., Reddy R., Aschner M., Lewis D.A., Mirnics K. Altered expression of genes involved in inflammation and apoptosis in frontal cortex in major depression. Mol. Psychiatry 2011, 16:751-762.
68. Speisman R.B., Kumar A., Rani A., Foster T.C., Ormerod B.K. Daily exercise improves memory, stimulates hippocampal neurogenesis and modulates immune and neuroimmune cytokines in aging rats. Brain Behav. Immun. 2012, 28:25-43.
69. Sugama S., Wirz S.A., Barr A.M., Conti B., Bartfai T., Shibasaki T. Interleukin-18 null mice show diminished microglial activation and reduced dopaminergic neuron loss following acute 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine treatment. Neuroscience 2004, 128:451-458.
70. Sugimoto N., Nakahira M., Ahn H.J., Micallef M., Hamaoka T., Kurimoto M., Fujiwara H. Differential requirements for JAK2 and TYK2 in T cell proliferation and IFN-gamma production induced by IL-12 alone or together with IL-18. Eur. J. Immunol. 2003, 33:243-251.
71. Sutinen E.M., Pirttilä T., Anderson G., Salminen A., Ojala J.O. Pro-inflammatory interleukin-18 increases Alzheimer's disease-associated amyloid-β production in human neuron-like cells. J. Neuroinflamm. 2012, 16(9):199.
72. Thomassen E., Bird T.A., Renshaw B.R., Kennedy M.K., Sims J.E. Binding of interleukin-18 to the interleukin-1 receptor homologous receptor IL-1Rrp1 leads to activation of signaling pathways similar to those used by interleukin-1. J. Interferon Cytok. Res. 1998, 18:1077-1088.
73. Tsuji-Takayama K., Aizawa Y., Okamoto I., Kojima H., Koide K., Takeuchi M., Ikegami H., Ohta T., Kurimoto M. Interleukin-18 induces interferon-gamma production through NF-kappaB and NFAT activation in murine T helper type 1 cells. Cell. Immunol. 1999, 196:41-50.
74. Yaguchi T., Nagata T., Yang D., Nishizaki T. Interleukin-18 regulates motor activity, anxiety and spatial learning without affecting synaptic plasticity. Behav. Brain Res. 2010, 20:47-51.
75. Yu X.H., Jiang H.L., Chen W.J., Yin K., Zhao G.J., Mo Z.C., Ouyang X.P., Lv Y.C., Jiang Z.S., Zhang D.W., Tang C.K. Interleukin-18 and interleukin-12 together downregulate ATP-binding cassette transporter A1 expression through the interleukin-18R/nuclear factor-κB signaling pathway in THP-1 macrophage-derived foam cells. Circ. J. 2012, 76:1780-1791.
76. Viatour P., Merville M.P., Bours V., Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 2005, 30:43-52.
77. von Giesen H.J., Jander S., Köller H., Arendt G. Serum and cerebrospinal fluid levels of interleukin-18 in human immunodeficiency virus type 1-associated central nervous system disease. J. Neurovirol. 2004, 10:383-386.
78. Zalcman S., Green-Johnson J.M., Murray L., Nance D.M., Dyck D., Anisman H., Greenberg A.H. Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6. Brain Res. 1994, 643:40-49.
79. Zhang X.M., Duan R.S., Chen Z., Quezada H.C., Mix E., Winblad B., Zhu J. IL-18 deficiency aggravates kainic acid-induced hippocampal neurodegeneration in C57BL/6 mice due to an overcompensation by IL-12. Exp. Neurol. 2007, 205:64-73.
80. Wakahara R., Kunimoto H., Tanino K., Kojima H., Inoue A., Shintaku H., Nakajima K. Phospho-Ser727 of STAT3 regulates STAT3 activity by enhancing dephosphorylation of phospho-Tyr705 largely through TC45. Genes Cells 2012, 17:132-145.