Interleukin (IL)-10 inhibits IL-6 production in microglia by preventing activation of NF-κB

Molecular Brain Research

Volumn 77, Issue 1, 2000, Pages 138-147

  Heyen, Jonathan R R ^a   Ye, Shi ming ^a   Finck, Brian N ^a   Johnson, Rodney W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Interleukin 10; Interleukin 6; Lipopolysaccharide; Microglia; NF B

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; IMMUNOCYTOCHEMISTRY; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; TRANSCRIPTION REGULATION;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL LINE; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; GENE EXPRESSION REGULATION; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; MICROGLIA; NF-KAPPA B; TOSYLLYSINE CHLOROMETHYL KETONE; TOSYLPHENYLALANYL CHLOROMETHYL KETONE;

ANIMALIA; MURINAE;

EID: 0034646787     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(00)00042-5     Document Type: Article

References (51)

1. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 6:1990;1897-1906.
2. Bell M.J., Kochanek P.M., Doughty L.A., Carcillo J.A., Adelson P.D., Clark R.S., Wisniewski S.R., Whalen M.J., Dekosky S.T. Interleukin-6 and interleukin-10 in cerebrospinal fluid after severe traumatic brain injury in children. J. Neurotrauma. 14:1997;451-457.
3. Blum-Degen D., Muller T., Kuhn W., Gerlach M., Pruzuntek H., Riederer P. Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci. Lett. 202:1995;17-20.
4. Bluthe R.M., Castanon N., Pousset F., Bristow A., Ball C., Lestage J., Michaud B., Kelley K.W., Dantzer R. Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats. Psychoneuroendocrinology. 3:1999;301-311.
5. Campbell I.L., Abraham C.R., Masliah E., Kemper P., Inglis J.D., Oldstone M.B.A., Mucke L. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc. Natl. Acad. Sci. USA. 90:1993;10061-10065.
6. Cassatella M.A., Meda L., Gasperini S., Calzetti F., Bonora S. Interleukin-10 upregulates IL-1 receptor antagonist production from lipopolysaccharide-stimulated human polymorphonuclear leukocytes by deleting mRNA degradation. J. Exp. Med. 179:1994;1695-1699.
7. Chai Z., Gatti S., Toniatti C., Poli V., Bartfai T. Interleukin-6 gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL-1β; a study on IL-6 deficient mice. J. Exp. Med. 183:1996;311-316.
8. de Waal Malefyt R., Abrams J., Bennett B., Figdor C.G., de Vries J.E. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1991;1209-1220.
9. Dendorfer U., Oettgen P., Libermann T.A. Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol. Cell. Biol. 14:1994;4443-4454.
10. Dickensheets H.L., Freeman S.L., Smith M.F., Donnely R.P. Interleukin-10 upregulates tumor necrosis factor type-II (p75) gene expression in endotoxin-stimulated human monocytes. Blood. 90:1997;4162-4171.
11. Fattori E., Cappelletti M., Costa P., Sellitto C., Cantoni L., Faggioni R., Fantuzzi G., Ghezzi P., Poli V. Defective inflammatory response in interleukin-6-deficient mice. J. Exp. Med. 180:1994;1243-1250.
12. Fiorentino D.F., Zlotnik A., Mosmann T.R., Howard M., O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147:1991;3815-3822.
13. Gruol D.L., Nelson T.E. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol. Neurobiol. 15:1997;307-339.
14. Hans V.H.J., Kossmann T., Joller H., Otto V., Morganti-Kossmann M. Interleukin-6 and its soluble receptor in serum and cerebrospinal fluid after cerebral trauma. Neuroreport. 10:1999;409-412.
15. Henkel T., Machleidt T., Alkalay I., Kronke M., Ben-Neriah Y., Baeuerle P.A. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature. 365:1993;182-185.
16. Heyser C.J., Masliah E., Samimi A., Campbell I.L., Gold L.H. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc. Natl. Acad. Sci. USA. 94:1997;1500-1505.
17. Kim H., Lee H.S., Chang K.T., Ko T.H., Baek K.J., Kwon N.S. Cholomethyl ketones block induction of nitric oxide synthase in murine macrophages by preventing activation of nuclear factor-kappa B. J. Immunol. 154:1995;4741-4748.
18. Klir J.J., Roth J., Szelenyi Z., McCellan J.L., Kluger M.J. Role of hypothalamic interleukin-6 and tumor necrosis factor-alpha in LPS fever in rats. Am J. Physiol. 265:1993;R512-R517.
19. Knoblach S.M., Faden A.I. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental brain injury. Exp. Neurol. 153:1998;143-151.
20. Kossmann T., Hans V., Imhof H.G., Stocker R., Grob P., Trentz O., Morganti-Kossmann M.C. Intrathecal and serum interleukin-6 and the acute phase response in patients with severe traumatic brain injuries. Shock. 5:1995;311-317.
21. Kossmann T., Hans V., Imhof H.G., Trentz O., Morganti-Kossmann M.C. Interleukin-6 released in human cerebral fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res. 25:1996;143-152.
22. Kozak W., Poli V., Soszynski D., Conn C.A., Leon L.R., Kluger M.J. Sickness behavior in mice deficient in interleukin-6 during turpentine abscess and influenza pneumonitis. Am. J. Physiol. 272:1997;R621-R630.
23. 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. Mol. Brain Res. 27:1994;157-162.
24. Lenczowski M., Bluthe R.-M., Roth J., Rees G., Rushforth D., Van Dam A., Tilders F., Rothwell N.J., Luheshi G. Central administration of rat IL-6 induces HPA axis activation and fever but not sickness behavior in rats. Am. J. Physiol. 276:1999;R652-R658.
25. Leon L.R., Kozak W., Rudolph K., Kluger M.J. An antipyretic role for interleukin-10 in LPS fever in mice. Am. J. Physiol. 276:1999;R81-R89.
26. Libermann T.A., Baltimore D. Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10:1990;2327-2334.
27. Matsusaka T., Fujikawa K., Nishio N., Mukaida N., Matsyshima K., Kishimoto T., Akira S. Transcriptions factors NF-IL6 and NF-κB synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8. Proc. Natl. Acad. Sci. USA. 90:1993;10193-10197.
28. Mogi M., Harada M., Narabayashi H., Inagaki H., Minami M., Nagatsu T. Interleukin (IL)-1 beta, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease. Neurosci. Lett. 211:1996;13-16.
29. Nava F., Calapai G., Facciola G., Cuzzocrea S., Marciano M.C., De Sarro A., Caputi A.P. Effects of IL-10 on water intake, locomotor activity, and rectal temperature in rat treated with endotoxin. Int. J. Immunopharmacol. 1:1997;31-38.
30. Oka T., Oka K., Hosio M., Hori T. Intracerebroventricular injection of interleukin-6 induces thermal hyperalgesia in rats. Brain Res. 692:1995;123-128.
31. Perlstein R.S., Whitnall M.H., Abrams J.S., Mougey E.H., Neta R. Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology. 132:1993;946-952.
32. Plata-Salaman C.R. Anorexia induced by activators of the signal transducer gp 130. Neuroreport. 7:1996;841-844.
33. Ray A., LaForge K.S., Sehgal P.B. On the mechanism for efficient repression of the interleukin-6 promoter by glucocorticoids: enhancer, TATA box and RNA start site (Inr motif) occlusion. Mol. Cell. Biol. 11:1990;5736-5746.
34. Righi M., Mori L., De Libero G., Sironi M., Biondi A., Mantovani A., Donini S.D., Ricciardi-Castagnoli P. Monokine production by microglial cell clones. Eur. J. Immunol. 19:1989;1443-1448.
35. Rothwell N.J., Busbridge N.J., Lefeuvre R.A., Hardwick A.J., Gauldie J., Hopkins S.J. Interleukin-6 is an central acting endogenous pyrogenin the rat. Can J. Physiol. Pharmacol. 69:1991;1465-1469.
36. N.J. Rothwell, S. Allan, Toulmond, The role of interleukin-1 in acute neurodegeration and stroke: pathophysiological and therapeutic implications, J. Clin. Inv. 100 (1997) 2648-2652.
37. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual, 2nd Edition, Cold Spring Harbor Laboratory,. Cold Spring Harbor, NY. (1989) pp. 10.59-10.63, 11.31-11.34.
38. SAS. (1990) SAS/STAT User's Guide, Version 6, SAS Institute, Cary, NC.
39. Sawada M., Suzumura A., Hosoya H., Marunouchi T., Nagatsu T. Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 72:1999;1466-1471.
40. Sheng W.S., Hu S., Kravitz F.H., Peterson P.K., Chao C.C. Tumor necrosis factor alpha upregulates human microglial cell production of interleukin-10 in vitro. Clin. Diagn. Lab. Immunol. 2:1995;604-608.
41. Shimizu H., Mitomo K., Watanabe T., Okamoto S., Yamamoto K. Involvement of a NF-κB-like transcription factor in the activation of the interleukin-6 gene by inflammatory lymphokines. Mol. Cell. Biol. 10:1990;561-568.
42. Spera P.A., Ellison J.A., Feuerstein G.Z., Barone F.C. IL-10 reduces rat brain injury following stroke. Neurosci. Lett. 31:1998;189-192.
43. Takeshita S., Gage J.R., Kishimoto T., Vredevoe D.L., Martinez-Maza O. Differential regulation of IL-6 gene transcription and expression by IL-4 and IL-10 in human monocytic cell lines. J. Immunol. 156:1996;2591-2598.
44. Tanabe O., Akira S., Kamiys T., Wong G.G., Hirano T., Kishimoto T. Genomic structure of the murine IL-6 gene, High degree conservation of potential regulatory sequences between mouse and human. J. Immunol. 141:1988;3875-3881.
45. Tilg H., Dinarello C.A., Mier J.W. IL-6 and APPs: anti-inflammatory and immunosuppressive mediators. Immunol. Today. 18:1997;428-432.
46. Toliver-Kinsky T., Papaconstantinou J., Perez-Polo J.R. Age-associated alterations in hippocampal and basal forebrain nuclear factor kappa B activity. J. Neurosci. Res. 48:1997;580-587.
47. Wang P., Wu P., Siegel M.I., Egan R.W., Motasim Billah M. IL-10 inhibits transcription of cytokine genes in human peripheral blood mononuclear cells. J. Immunol. 153:1994;811-816.
48. Wong M.L., Bongiorno P.B., Rettori V., McCann S.M., Licinio J. Interleukin (IL)-1β, IL-1 receptor antagonist, IL-10 and IL-13 gene expression in the central nervous system and anterior pituitary during systemic inflammation: Pathophysiological implications. Proc. Natl. Acad. Sci. USA. 90:1994;227-232.
49. Yao J., Johnson R.W. Induction of interleukin-1 beta-converting enzyme (ICE) in murine microglia by lipopolysaccharide. Mol. Brain. Res. 51:1997;170-178.
50. Ye S.M., Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. J. Immunol. 93:1999;139-148.
51. Zhang Y.H., Lin J.X., Vilcek J. Interleukin-6 induction by tumor necrosis factor and interleukin-1 in human fibroblasts involves activation of a nuclear factor binding to a nuclear factor binding to a kappa B-like sequence. Mol. Cell. Biol. 10:1990;3818-3823.