LPS-induced release of IL-6 from glia modulates production of IL-1β in a JAK2-dependent manner

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Minogue, Aedín M ^a   Barrett, James P ^a   Lynch, Marina A ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Glia; Neuroinflammation; SOCS3; STAT1; TNFR1

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE 2; LIPOPOLYSACCHARIDE; N TERT BUTYL 3 [5 METHYL 2 [4 (4 METHYL 1 PIPERAZINYL)PHENYLAMINO] 4 PYRIMIDINYLAMINO]BENZENESULFONAMIDE; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; GLIA; IMMUNOMODULATION; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION;

EID: 84862189232     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-126     Document Type: Article

References (46)

1. Benarroch EE. Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin Proc 2005, 80:1326-1338. 10.4065/80.10.1326, 16212146.
2. Cacabelos R, Alvarez XA, Franco-Maside A, Fernandez-Novoa L, Caamano J. Serum tumor necrosis factor (TNF) in Alzheimer's disease and multi-infarct dementia. Methods Find Exp Clin Pharmacol 1994, 16:29-35.
3. McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291. 10.1212/WNL.38.8.1285, 3399080.
4. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL, Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci U S A 1989, 86:7611-7615. 10.1073/pnas.86.19.7611, 298116, 2529544.
5. Wood JA, Wood PL, Ryan R, Graff-Radford NR, Pilapil C, Robitaille Y, Quirion R. Cytokine indices in Alzheimer's temporal cortex: no changes in mature IL-1 beta or IL-1RA but increases in the associated acute phase proteins IL-6, alpha 2-macroglobulin and C-reactive protein. Brain Res 1993, 629:245-252. 10.1016/0006-8993(93)91327-O, 7509248.
6. Galanos C, Freudenberg MA. Mechanisms of endotoxin shock and endotoxin hypersensitivity. Immunobiology 1993, 187:346-356. 10.1016/S0171-2985(11)80349-9, 8330903.
7. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004, 173:3916-3924.
8. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN. LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1alpha in macrophages and microglia. Blood 2005, 106:3114-3122. 10.1182/blood-2005-02-0759, 1895321, 16020513.
9. Kurzer JH, Argetsinger LS, Zhou YJ, Kouadio JL, O'Shea JJ, Carter-Su C. Tyrosine 813 is a site of JAK2 autophosphorylation critical for activation of JAK2 by SH2-B beta. Mol Cell Biol 2004, 24:4557-4570. 10.1128/MCB.24.10.4557-4570.2004, 400461, 15121872.
10. Oh JW, Van Wagoner NJ, Rose-John S, Benveniste EN. Role of IL-6 and the soluble IL-6 receptor in inhibition of VCAM-1 gene expression. J Immunol 1998, 161:4992-4999.
11. Nolan Y, Martin D, Campbell VA, Lynch MA. Evidence of a protective effect of phosphatidylserine-containing liposomes on lipopolysaccharide-induced impairment of long-term potentiation in the rat hippocampus. J Neuroimmunol 2004, 151:12-23. 10.1016/j.jneuroim.2004.02.001, 15145599.
12. Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KH, Lynch MA. CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci 2007, 27:8309-8313. 10.1523/JNEUROSCI.1781-07.2007, 17670977.
13. Bacon CM, McVicar DW, Ortaldo JR, Rees RC, O'Shea JJ, Johnston JA. Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J Exp Med 1995, 181:399-404. 10.1084/jem.181.1.399, 2191828, 7528775.
14. Parganas E, Wang D, Stravopodis D, Topham DJ, Marine JC, Teglund S, Vanin EF, Bodner S, Colamonici OR, van Deursen JM, Grosveld G, Ihle JN. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 1998, 93:385-395. 10.1016/S0092-8674(00)81167-8, 9590173.
15. Jones SA. Directing transition from innate to acquired immunity: defining a role for IL-6. J Immunol 2005, 175:3463-3468.
16. Samoilova EB, Horton JL, Hilliard B, Liu TS, Chen Y. IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J Immunol 1998, 161:6480-6486.
17. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Kohler G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994, 368:339-342. 10.1038/368339a0, 8127368.
18. Fattori E, Cappelletti M, Costa P, Sellitto C, Cantoni L, Carelli M, Faggioni R, Fantuzzi G, Ghezzi P, Poli V. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med 1994, 180:1243-1250. 10.1084/jem.180.4.1243, 2191674, 7931061.
19. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, Lei XF, Achong MK. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest 1998, 101:311-320. 10.1172/JCI1368, 508569, 9435302.
20. Pardanani A, Hood J, Lasho T, Levine RL, Martin MB, Noronha G, Finke C, Mak CC, Mesa R, Zhu H, Soll R, Gilliland DG, Tefferi A. TG101209, a small molecule JAK2-selective kinase inhibitor potently inhibits myeloproliferative disorder-associated JAK2V617F and MPLW515L/K mutations. Leukemia 2007, 21:1658-1668. 10.1038/sj.leu.2404750, 17541402.
21. Ramakrishnan V, Kimlinger T, Haug J, Timm M, Wellik L, Halling T, Pardanani A, Tefferi A, Rajkumar SV, Kumar S. TG101209, a novel JAK2 inhibitor, has significant in vitro activity in multiple myeloma and displays preferential cytotoxicity for CD45+ myeloma cells. Am J Hematol 2010, 85:675-686. 10.1002/ajh.21785, 2940994, 20652971.
22. Wang Y, Fiskus W, Chong DG, Buckley KM, Natarajan K, Rao R, Joshi A, Balusu R, Koul S, Chen J, Savoie A, Ustun C, Jillella AP, Atadja P, Levine RL, Bhalla KN. Cotreatment with panobinostat and JAK2 inhibitor TG101209 attenuates JAK2V617F levels and signaling and exerts synergistic cytotoxic effects against human myeloproliferative neoplastic cells. Blood 2009, 114:5024-5033. 10.1182/blood-2009-05-222133, 2788976, 19828702.
23. Sun Y, Moretti L, Giacalone NJ, Schleicher S, Speirs CK, Carbone DP, Lu B. Inhibition of JAK2 signaling by TG101209 enhances radiotherapy in lung cancer models. J Thorac Oncol 2011, 6:699-706. 10.1097/JTO.0b013e31820d9d11, 3104103, 21325979.
24. Manderson AP, Kay JG, Hammond LA, Brown DL, Stow JL. Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFalpha. J Cell Biol 2007, 178:57-69. 10.1083/jcb.200612131, 2064421, 17606866.
25. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol 1999, 17:331-367. 10.1146/annurev.immunol.17.1.331, 10358762.
26. Baud V, Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001, 11:372-377. 10.1016/S0962-8924(01)02064-5, 11514191.
27. Hehlgans T, Pfeffer K. The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 2005, 115:1-20. 10.1111/j.1365-2567.2005.02143.x, 1782125, 15819693.
28. Chen P, Huang L, Zhang Y, Qiao M, Yao W, Yuan Y. The antagonist of the JAK-1/STAT-1 signaling pathway improves the severity of cerulein-stimulated pancreatic injury via inhibition of NF-kappaB activity. Int J Mol Med 2011, 27:731-738.
29. Funakoshi-Tago M, Tago K, Sato Y, Tominaga S, Kasahara T. JAK2 is an important signal transducer in IL-33-induced NF-kappaB activation. Cell Signal 2011, 23:363-370. 10.1016/j.cellsig.2010.10.006, 20940045.
30. Qi XF, Kim DH, Yoon YS, Jin D, Huang XZ, Li JH, Deung YK, Lee KJ. Essential involvement of cross-talk between IFN-gamma and TNF-alpha in CXCL10 production in human THP-1 monocytes. J Cell Physiol 2009, 220:690-697. 10.1002/jcp.21815, 19472212.
31. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements JM, Crimmin M, Davidson AH, Drummond AH, Galloway WA, Gilbert R, Gordon JL, Leber TM, Mangan M, Miller K, Nayee P, Owen K, Patel S, Thomas W, Wells G, Wood LM. Woolley, K:l. Matrix metalloproteinases and processing of pro-TNF-alpha. J Leukoc Biol 1995, 57:774-777.
32. Argetsinger LS, Campbell GS, Yang X, Witthuhn BA, Silvennoinen O, Ihle JN, Carter-Su C. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 1993, 74:237-244. 10.1016/0092-8674(93)90415-M, 8343952.
33. Fuortes M, Jin WW, Nathan C. Adhesion-dependent protein tyrosine phosphorylation in neutrophils treated with tumor necrosis factor. J Cell Biol 1993, 120:777-784. 10.1083/jcb.120.3.777, 2119542, 8425901.
34. Fuortes M, Jin WW, Nathan C. Beta 2 integrin-dependent tyrosine phosphorylation of paxillin in human neutrophils treated with tumor necrosis factor. J Cell Biol 1994, 127:1477-1483. 10.1083/jcb.127.5.1477, 2120254, 7525608.
35. Fuortes M, Melchior M, Han H, Lyon GJ, Nathan C. Role of the tyrosine kinase pyk2 in the integrin-dependent activation of human neutrophils by TNF. J Clin Invest 1999, 104:327-335. 10.1172/JCI6018, 408415, 10430614.
36. Mishra S, Mathur R, Hamburger AW. Modulation of the cytotoxic activity of tumor necrosis factor by protein tyrosine kinase and protein tyrosine phosphatase inhibitors. Lymphokine Cytokine Res 1994, 13:77-83.
37. Takada Y, Aggarwal BB. TNF activates Syk protein tyrosine kinase leading to TNF-induced MAPK activation, NF-kappaB activation, and apoptosis. J Immunol 2004, 173:1066-1077.
38. Pincheira R, Castro AF, Ozes ON, Idumalla PS, Donner DB. Type 1 TNF receptor forms a complex with and uses Jak2 and c-Src to selectively engage signaling pathways that regulate transcription factor activity. J Immunol 2008, 181:1288-1298.
39. Wang M, Markel T, Crisostomo P, Herring C, Meldrum KK, Lillemoe KD, Meldrum DR. Deficiency of TNFR1 protects myocardium through SOCS3 and IL-6 but not p38 MAPK or IL-1beta. Am J Physiol Heart Circ Physiol 2007, 292:H1694-H1699.
40. Eriksson U, Kurrer MO, Schmitz N, Marsch SC, Fontana A, Eugster HP, Kopf M. Interleukin-6-deficient mice resist development of autoimmune myocarditis associated with impaired upregulation of complement C3. Circulation 2003, 107:320-325. 10.1161/01.CIR.0000043802.38699.66, 12538435.
41. Ohshima S, Saeki Y, Mima T, Sasai M, Nishioka K, Nomura S, Kopf M, Katada Y, Tanaka T, Suemura M, Kishimoto T. Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc Natl Acad Sci U S A 1998, 95:8222-8226. 10.1073/pnas.95.14.8222, 20957, 9653168.
42. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, De Benedetti F, Poli V, Ciliberto G. Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 1998, 187:461-468. 10.1084/jem.187.4.461, 2212160, 9463396.
43. Deng C, Goluszko E, Tuzun E, Yang H, Christadoss P. Resistance to experimental autoimmune myasthenia gravis in IL-6-deficient mice is associated with reduced germinal center formation and C3 production. J Immunol 2002, 169:1077-1083.
44. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 1994, 83:113-118.
45. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, Hirano T, Chien KR, Yoshimura A. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 2003, 4:551-556. 10.1038/ni938, 12754507.
46. Lynch AM, Walsh C, Delaney A, Nolan Y, Campbell VA, Lynch MA. Lipopolysaccharide-induced increase in signalling in hippocampus is abrogated by IL-10-a role for IL-1 beta?. J Neurochem 2004, 88:635-646. 10.1046/j.1471-4159.2003.02157.x, 14720213.