Interferon-γ differentially modulates the release of cytokines and chemokines in lipopolysaccharide- and pneumococcal cell wall-stimulated mouse microglia and macrophages

European Journal of Neuroscience

Volumn 16, Issue 11, 2002, Pages 2113-2122

  Häusler, Karl Georg ^a   Prinz, Marco ^b   Nolte, Christiane ^a   Weber, Joerg R ^c   Schumann, Ralf R ^d   Kettenmann, Helmut ^a   Hanisch, Uwe Karsten ^a,e  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e Lausitz University of Applied Sciences   (Germany)

Author keywords

Inflammation; JAK; Monocytes macrophages; Priming; S. pneumoniae

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; ONCOPROTEIN; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; LEUKOCYTE; MACROPHAGE; MICROGLIA; MOUSE; NEUROIMMUNOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL COMMUNICATION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALITIS; FEEDBACK; INTERFERON TYPE II; INTERLEUKIN-12; LIPOPOLYSACCHARIDES; MACROPHAGES; MENINGITIS, PNEUMOCOCCAL; MICE; MICROGLIA; POLYSACCHARIDES, BACTERIAL; RANTES;

EID: 18744390011     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02287.x     Document Type: Article

References (86)

1. Allan, S.M. & Rothwell, N.J. (2001) Cytokines and acute neurodegeneration. Nature Rev. Neurosci., 2, 734-744.
2. Aloisi, F. (2001) Immune function of microglia. Glia, 36, 165-179.
3. Asensio, V.C. & Campbell, I.L. (1999) Chemokines in the CNS: Plurifunctional mediators in diverse states. Trends Neurosci., 22, 504-512.
4. Bacon, K.B. & Harrison, J.K. (2000) Chemokines and their receptors in neurobiology: Perspectives in physiology and homeostasis. J. Neuroimmunol., 104, 92-97.
5. Bajetto, A., Bonavia, R., Barbero, S., Florio, T. & Schettini, G. (2001) Chemokines and their receptors in the central nervous system. Front. Neuroendocrinol., 22, 147-184.
6. abd-el Basset, E. & Fedoroff, S. (1995) Effect of bacterial wall lipopolysaccharide (LPS) on morphology, motility, and cytoskeletal organization of microglia in cultures. J. Neurosci. Res., 41, 222-237.
7. Becher, B., Prat, A. & Antel, J.P. (2000) Brain-immune connection: Immunoregulatory properties of CNS-resident cells. Glia, 29, 293-304.
8. Bell, M.D., Taub, D.D., Kunkel, S.J., Strieter, R.M., Foley, R., Gauldie, J. & Perry, V.H. (1996) Recombinant human adenovirus with rat MIP-2 gene insertion causes prolonged PMN recruitment to the murine brain. Eur. J. Neurosci., 8, 1803-1811.
9. Biber, K., Zuurman, M.W., Dijkstra, I.M. & Boddeke, H.W.G.M. (2002) Chemokines in the brain: Neuroimmunology and beyond. Curr. Opin. Pharmacol., 2, 63-68.
10. Blasi, E., Puliti, M., Pitzurra, L., Bartoli, A. & Bistoni, F. (1994) Heterogeneous secretory response of phagocytes from different anatomical districts to the dimorphic fungus Candida albicans. Cell. Immunol., 153, 239-247.
11. Blasko, I., Ransmayr, G., Veerhuis, R., Eikelenboom, P. & Grubeck-Loebenstein, B. (2001) Does IFNgamma play a role in neurodegeneration? J. Neuroimmunol., 116, 1-4.
12. Blasko, I., Veerhuis, R., Stampfer-Kountchev, M., Saurwein-Teissl, M., Eikelenboom, P. & Grubeck-Loebenstein, B. (2000) Costimulatory effects of interferon-gamma and interleukin-1beta or tumor necrosis factor alpha on the synthesis of Abeta1-40 and Abeta1-42 by human astrocytes. Neurobiol. Dis., 7, 682-689.
13. Bocchini, V., Mazzolla, R., Blasi, E., Sick, P. & Kettenmann, H. (1992) An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res., 31, 616-621.
14. Boehm, U., Klamp, T., Groot, M. & Howard, J.C. (1997) Cellular responses to interferon-gamma. Annu. Rev. Immunol., 15, 749-795.
15. Bogdan, I., Leib, S.L., Bergeron, M., Chow, L. & Tauber, M.G. (1997) Tumor necrosis factor-alpha contributes to apoptosis in hippocampal neurons during experimental group B streptococcal meningitis. J. Infect. Dis., 176, 693-697.
16. Bohr, V., Paulson, O.B. & Rasmussen, N. (1984) Pneumococcal meningitis. Late neurologic sequelae and features of prognostic impact. Arch. Neurol., 41, 1045-1049.
17. Bright, J.J., Du, C. & Sriram, S. (1999) Tyrphostin B42 inhibits IL-12-induced tyrosine phosphorylation and activation of Janus kinase-2 and prevents experimental allergic encephalomyelitis. J. Immunol., 162, 6255-6262.
18. Brown, K.A. (2001) Factors modifying the migration of lymphocytes across the blood-brain barrier. Int. Immunopharmacol., 1, 2043-2062.
19. De Maeyer, E. & De Maeyer-Guignard, J. (1998) Interferons. In Thomson, A. (ed), The Cytokine Handbook, Academic Press, San Diego, pp. 491-516.
20. Diab, A., Abdalla, H., Li, H.L., Shi, F.D., Zhu, J., Hojberg, B., Lindquist, L., Wretlind, B., Bakhiet, M. & Link, H. (1999) Neutralization of macrophage inflammatory protein 2 (MIP-2) and MIP-1alpha attenuates neutrophil recruitment in the central nervous system during experimental bacterial meningitis. Infect. Immunol., 67, 2590-2601.
21. + channels in mouse brain microglia: Cells acquire responsiveness to pneumococcal cell wall components during late development. Neuroscience, 89, 1379-1390.
22. Durand, M.L., Calderwood, S.B., Weber, D.J., Miller, S.I., Southwick, F.S., Caviness, V.S. Jr & Swartz, M.N. (1993) Acute bacterial meningitis in adults. A review of 493 episodes. N. Engl. J. Med., 328, 21-28.
23. Fassbender, K., Mielke, O., Bertsch, T., Muehlhauser, F., Hennerici, M., Kurimoto, M. & Rossol, S. (1999) Interferon-gamma-inducing factor (IL-18) and interferon-gamma in inflammatory CNS diseases. Neurology, 53, 1104-1106.
24. Freyer, D., Manz, R., Ziegenhorn, A., Weih, M., Angstwurm, K., Döcke, W.D., Meisel, A., Schumann, R.R., Schönfelder, G., Dirnagl, U. & Weber, J.R. (2000) Cerebral endothelial cells release TNFα after stimulation with cell walls of Streptococcus pneumoniae and regulate iNOS and ICAM-1 expression via autocrine loops. J. Immunol., 163, 4308-4314.
25. Gonzalez-Scarano, F. & Baltuch, G. (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci., 22, 219-240.
26. Gu, L., Rutledge, B., Fiorillo, J., Ernst, C., Grewal, I., Flavell, R., Gladue, R. & Rollins, B. (1997) In vivo properties of monocyte chemoattractant protein-1. J. Leukoc. Biol., 62, 577-580.
27. Guha, M. & Mackman, N. (2001) LPS induction of gene expression in human monocytes. Cell Signal., 13, 85-94.
28. Hallam, D.M., Capps, N.L., Travelstead, A.L., Brewer, G.J. & Maroun, L.E. (2000) Evidence for an interferon-related inflammatory reaction in the trisomy 16 mouse brain leading to caspase-1-mediated neuronal apoptosis. J. Neuroimmunol., 110, 66-75.
29. Hanisch, U.K. (2001a) Effects of interleukin-2 and interferons on the nervous system. In Ader, R. Felten, D.L. & Cohen, N. (eds), Psychoneuroimmunology Academic Press, San Diego, pp. 585-631.
30. Hanisch, U.K. (2001b) Microglia as a source and target of cytokine activities in the brain. In Streit, W.J. (ed), Microglia in the Degenerating and Regenerating CNS, Springer-Verlag, New York, pp. 79-124.
31. Hanisch, U.K., Prinz, M., Angstwurm, K., Hausler, K.G., Kann, O., Kettenmann, H. & Weber, J.R. (2001) The protein tyrosine kinase inhibitor AG126 prevents the massive microglial cytokine induction by pneumococcal cell walls. Eur. J. Immunol., 31, 2104-2115.
32. Hesselgesser, J. & Horuk, R. (1999) Chemokine and chemokine receptor expression in the central nervous system. J. Neurovirol., 5, 13-26.
33. Hua, L.L. & Lee, S.C. (2000) Distinct patterns of stimulus-inducible chemokine mRNA accumulation in human fetal astrocytes and microglia. Glia, 30, 74-81.
34. Huang, D.R., Wang, J., Kivisakk, P., Rollins, B.J. & Ransohoff, R.M. (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med., 193, 713-726.
35. Ingraham, J.L., Maaloe, O. & Neidhardt, F.C. (1983) Growth of the Bacterial Cell. Sinauer Associates, Inc, Sunderland.
36. Kawai, T., Seki, M., Hiromatsu, K., Eastcott, J.W., Watts, G.F., Sugai, M., Smith, D.J., Porcelli, S.A. & Taubman, M.A. (1999) Selective diapedesis of Th1 cells induced by endothelial cell RANTES. J. Immunol., 163, 3269-3278.
37. Kielian, T., Barry, B. & Hickey, W.F. (2001) CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J. Immunol., 166, 4634-4643.
38. Kim, Y.S. & Tauber, M.G. (1996) Neurotoxicity of glia activated by Gram-positive bacterial products depends on nitric oxide production. Infect. Immunol., 64, 3148-3153.
39. Koerner, T.J., Adams, D.O. & Hamilton, T.A. (1987) Regulation of tumor necrosis factor (TNF) expression: Interferon-gamma enhances the accumulation of mRNA for TNF induced by lipopolysaccharide in murine peritoneal macrophages. Cell Immunol., 109, 437-443.
40. Kopydlowski, K.M., Salkowski, C.A., Cody, M.J., van Rooijen, N., Major, J., Hamilton, T.A. & Vogel, S.N. (1999) Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J. Immunol., 163, 1537-1544.
41. Li, H.L., Kostulas, N., Huang, Y.M., van der Xiao, B.G.M.P., Kostulas, V., Giedraitas, V. & Link, H. (2001) IL-17 and IFN-gamma mRNA expression is increased in the brain and systemically after permanent middle cerebral artery occlusion in the rat. J. Neuroimmunol., 116, 5-14.
42. Lorsbach, R.B., Murphy, W.J., Lowenstein, C.J., Snyder, S.H. & Russell, S.W. (1993) Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-gamma and lipopolysaccharide. J. Biol. Chem., 268, 1908-1913.
43. Luster, A.D. (1998) Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med., 338, 436-445.
44. Luther, S.A. & Cyster, J.G. (2001) Chemokines as regulators of T cell differentiation. Nature Immunol., 2, 102-107.
45. Mantovani, A. (1999) The chemokine system: Redundancy for robust outputs. Immunol. Today, 20, 254-257.
46. McManus, C.M., Brosnan, C.F. & Berman, J.W. (1998) Cytokine induction of MIP-1 alpha and MIP-1 beta in human fetal microglia. J. Immunol., 160, 1449-1455.
47. McManus, C.M., Liu, J.S., Hahn, M.T., Hua, L.L., Brosnan, C.F., Berman, J.W. & Lee, S.C. (2000) Differential induction of chemokines in human microglia by type I and II interferons. Glia, 29, 273-280.
48. Mennerick, S., Benz, A. & Zorumski, C.F. (1996) Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures. J. Neurosci., 16, 55-64.
49. Meydan, N., Grunberger, T., Dadi, H., Shahar, M., Arpaia, E., Lapidot, Z., Leeder, J.S., Freedman, M., Cohen, A., Gazit, A., Levitzki, A. & Roifman, C.M. (1996) Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature, 379, 645-648.
50. Möller, T., Nolte, C., Burger, R., Verkhratsky, A. & Kettenmann, H. (1997) Mechanisms of C5a and C3a complement fragment-induced [Ca2+]i signaling in mouse microglia. J. Neurosci., 17, 615-624.
51. Moser, B. & Loetscher, P. (2001) Lymphocyte traffic control by chemokines. Nature Immunol., 2, 123-128.
52. Nau, R. & Brück, W. (2002) Neuronal injury in bacterial meningitis: Mechanisms and implications for therapy. Trends Neurosci., 25, 38-45.
53. Neumann, H., Schmidt, H., Wilharm, E., Behrens, L. & Wekerle, H. (1997) Interferon gamma gene expression in sensory neurons: Evidence for autocrine gene regulation. J. Exp. Med., 186, 2023-2031.
54. Nörenberg, W., Gebicke-Haerter, P.J. & Illes, P. (1994) Voltage-dependent potassium channels in activated rat microglia. J. Physiol. (Lond.), 475, 15-32.
55. Persidsky, Y., Ghorpade, A., Rasmussen, J., Limoges, J., Liu, X.J., Stins, M., Fiala, M., Way, D., Kim, K.S., Witte, M.H., Weinand, M., Carhart, L. & Gendelman, H.E. (1999) Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am. J. Pathol., 155, 1599-1611.
56. Pfister, H.W., Feiden, W. & Einhäupl, K.M. (1993) Spectrum of complications during bacterial meningitis in adults. Results of a prospective clinical study. Arch. Neurol., 50, 575-581.
57. Polfliet, M.M.J., Zwijnenburg, P.J.G., van Furth, A.M., van der Poll, T., Döpp, E.A., de Lavalette, C.R., van Kesteren-Hendrikx, E.M.L., van Rooijen, N., Dijkstra, C.D. & van den Berg, T.K. (2001) Meningeal and perivascular macrophages of the central nervous system play a protective role during bacterial meningitis. J. Immunol., 167, 4644-4650.
58. Popko, B., Corbin, J.G., Baerwald, K.D., Dupree, J. & Garcia, A.M. (1997) The effects of interferon-gamma on the central nervous system. Mol. Neurobiol., 14, 19-35.
59. Prinz, M., Kann, O., Draheim, H.J., Schumann, R.R., Kettenmann, H., Weber, J.R. & Hanisch U.K. (1999) Microglial activation by components of Gram-positive and -negative bacteria: Distinct and common routes to the induction of ion channels and cytokines. J. Neuropathol. Exp. Neurol., 58, 1078-1089.
60. Raivich, G., Bohatschek, M., Kloss, C.U., Werner, A., Jones, L.L. & Kreutzberg, G.W. (1999) Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res. Rev., 30, 77-105.
61. Ring, A., Weiser, J.N. & Tuomanen, E.I. (1998) Pneumococcal trafficking across the blood-brain barrier. J. Clin. Invest., 102, 347-360.
62. Rothwell, N.J. (1997) Cytokines and acute neurodegeneration. Mol. Psychiatry, 2, 120-121.
63. Rothwell, N.J. & Luheshi, G.N. (2000) Interleukin 1 in the brain: Biology, pathology and therapeutic target. Trends Neurosci., 23, 618-625.
64. Rubin, L.L. & Staddon, J.M. (1999) The cell biology of the blood-brain barrier. Annu. Rev. Neurosci., 22, 11-28.
65. Sallusto, F., Lanzavecchia, A. & Mackay, C.R. (1998) Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol. Today, 19, 568-574.
66. Sande, M.A. & Täuber, M.G. (2001) Pneumococcal meningitis: Current pathophysiological concepts. In Tomasz,. (ed), Streptococcus Pneumoniae - Molecular Biology and Mechanisms of Disease Mary Ann Liebert, Inc, Larchmont, pp. 315-320.
67. Saurwein-Teissl, M., Blasko, I., Zisterer, K., Neuman, B., Lang, B. & Grubeck-Loebenstein, B. (2000) An imbalance between pro- and anti-inflammatory cytokines, a characteristic feature of old age. Cytokine, 12, 1160-1161.
68. Schumann, R.R., Leong, S.R., Flaggs, G.W., Gray, P.W., Wright, S.D., Mathison, J.C., Tobias, P.S. & Ulevitch, R.J. (1990) Structure and function of lipopolysaccharide binding protein. Science, 249, 1429-1431.
69. Sedgwick, J.D., Riminton, D.S., Cyster, J.G. & Körner, H. (2000) Tumor necrosis factor: A master-regulator of leukocyte movement. Immunol. Today, 21, 110-113.
70. Sherry, B., Espinoza, M., Manogue, K.R. & Cerami, A. (1998) Induction of the chemokine beta peptides, MIP-1 alpha and MIP-1 beta, by lipopolysaccharide is differentially regulated by immunomodulatory cytokines gamma-IFN, IL-10, IL-4, and TGF-beta. Mol. Med., 4, 648-657.
71. Siveke, J.T. & Hamann, A. (1998) T helper 1 and T helper 2 cells respond differentially to chemokines. J. Immunol., 160, 550-554.
72. Spanaus, K.S., Nadal, D., Pfister, H.W., Seebach, J., Widmer, U., Frei, K., Gloor, S. & Fontana, A. (1997) C-X-C and C-C chemokines are expressed in the cerebrospinal fluid in bacterial meningitis and mediate chemotactic activity on peripheral blood-derived polymorphonuclear and mononuclear cells in vitro. J. Immunol., 158, 1956-1964.
73. Sprenger, H., Rosler, A., Tonn, P., Braune, H.J., Huffmann, G. & Gemsa, D. (1996) Chemokines in the cerebrospinal fluid of patients with meningitis. Clin. Immunol. Immunopathol., 80, 155-161.
74. Stewart, C.C. (1981) Murine mononuclear phagocytes from bone marrow. In Adams, D.O. Edelson, P.J. & Koren, H. (eds), Methods for Studying Mononuclear Phagocytes, Academic Press, New York, pp. 5-20.
75. Stohwasser, R., Giesebrecht, J., Kraft, R., Müller, E.-C., Häusler, K.G., Kettenmann, H. & Hanisch U.K. & Kloetzel, P.-M. (2000) Biochemical analysis of proteasomes from microglia: Induction of immunoproteasomes by interferon-γ and lipopolysaccharide. Glia, 29, 355-365.
76. Streit, W.J., Walter, S.A. & Pennel, N.A. (2000) Reactive microgliosis. Prog. Neurobiol., 57, 563-581.
77. Tani, M., Fuentes, M.E., Peterson, J.W., Trapp, B.D., Durham, S.K., Loy, J.K., Bravo, R., Ransohoff, R.M. & Lira, S.A. (1996) Neutrophil infiltration, glial reaction, and neurological disease in transgenic mice expressing the chemokine N51/KC in oligodendrocytes. J. Clin. Invest., 98, 529-539.
78. Tran, E.H., Prince, E.N. & Owens, T. (2000) IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J. Immunol., 164, 2759-2768.
79. Tuomanen, E., Liu, H., Hengstler, B., Zak, O. & Tomasz, A. (1985) The induction of meningeal inflammation by components of the pneumococcal cell wall. J. Infect. Dis., 151, 859-868.
80. Tuomanen, E.I. & Masure, H.R. (1997) Molecular and cellular biology of pneumococcal infection. Microb. Drug Resist., 3, 297-308.
81. Ulevitch, R.J. & Tobias, P.S. (1995) Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol., 13, 437-457.
82. Verderio, C. & Matteoli, M. (2001) ATP mediates calcium signaling between astrocytes and microglial cells: Modulation by IFN-gamma. J. Immunol., 166, 6383-6391.
83. Weber, J.R., Angstwurm, K., Bürger, W., Einhäupl, K.M. & Dirnagl, U. (1995) Anti ICAM-1 (CD 54) monoclonal antibody reduces inflammatory changes in experimental bacterial meningitis. J. Neuroimmunol., 63, 63-68.
84. Wright, S.D., Ramos, R.A., Tobias, P.S., Ulevitch, R.J. & Mathison, J.C. (1990) CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science, 249, 1431-1433.
85. Xiao, B.G. & Link, H. (1998) IFN-gamma production of adult rat astrocytes triggered by TNF-alpha. Neuroreport, 9, 1487-1490.
86. Zujovic, V., Benavides, J., Vige, X., Carter, C. & Taupin, V. (2000) Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia, 29, 305-315.