Astrocytes enhance lipopolysaccharide-induced nitric oxide production by microglial cells

European Journal of Neuroscience

Volumn 16, Issue 7, 2002, Pages 1275-1283

  Solà, Carme ^a   Casal, Carme ^a   Tusell, Josep M ^a   Serratosa, Joan ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Glial interaction; Immunocytochemistry; Inducible nitric oxide synthase; Rat glial cell cultures

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BIOCHEMICAL MARKER; ISOENZYME; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ASSAY; CELL FUNCTION; CELL MEMBRANE; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ASSAY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MICROGLIA; NERVE CELL CULTURE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; RAT;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL COMMUNICATION; CELL MEMBRANE; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MICROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; RATS;

EID: 0036429923     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02199.x     Document Type: Article

References (59)

1. Acarín, L., González, B., Castellano, B. & Castro, A.J. (1996) Microglial response to N-methyl-D-aspartate-mediated excitotoxicity in the immature rat brain. J. Comp. Neurol., 367, 361-374.
2. Akiyama, H., Tooyama, I., Kondo, H., Ikeda, K., Kimura, H., McGeer, E.G. & McGeer, P.L. (1994) Early response of brain resident microglia to kainic acid-induced hippocampal lesions. Brain Res., 635, 257-268.
3. Aloisi, F., Borsellino, G., Caré, A., Testa, U., Gallo, P., Russo, G., Peschle, C. & Levi, G. (1995) Cytokine regulation of astrocyte function: In vitro studies using cells from the human brain. Int. J. Dev. Neurosci., 13, 265-274.
4. Barron, K.D., Marciano, F.F., Amundson, R. & Mankes, R. (1990) Perineuronal glial responses after axotomy of central and peripheral axons. A comparison. Brain Res., 523, 219-229.
5. van den Berg, K.J. & Gramsbergen, J.B.P. (1993) Long-term changes in glial (r)brillary acidic protein and calcium levels in rat hippocampus after a single systemic dose of kainic acid. Ann. NY Acad. Sci., 679, 394-401.
6. Boje, K.M. & Arora, P.K. (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res., 587, 250- 256.
7. Casal, C., Tusell, J.M. & Serratosa, J. (2001) Role of calmodulin in the differentiation/activation of microglial cells. Brain Res., 902, 101-107.
8. Chao, C.C., Hu, S., Molitor, T.W., Shaskann, E.G. & Peterson, P.K. (1992) Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol., 149, 2736-2741.
9. Chao, C.C., Hu, S. & Peterson, P.K. (1995) Glia, cytokines and neurotoxicity. Crit. Rev. Neurobiol., 9, 189-205.
10. Chen, C.C., Wang, J.K., Chen, W.C. & Lin, S.B. (1998) Protein kinase C η mediates lipopolysaccharide-induced nitric-oxide synthase expression in primary astrocytes. J. Biol. Chem., 272, 19424-19430.
11. Chung, I.Y. & Benveniste, E.N. (1990) Tumor necrosis factor α production by astrocytes. Induction by lipopolysaccharide, IFN-γ, and IL-1β. J. Immunol., 144, 2999-3007.
12. De Simone, R., Levi, G. & Aloisi, F. (1998) Interferon gamma gene expression in rat central nervous system glial cells. Cytokine, 10, 418-422.
13. Delacourte, A. (1990) General and dramatic glial reaction in Alzheimer brains. Neurology, 40, 33-37.
14. Eder, C., Schilling, T., Heineman, U., Haas, D., Hailer, N. & Nitsch, R. (1999) Morphological, immunophenotypical and electrophysiological properties of resting microglia in vitro. Eur. J. Neurosci., 11, 4251-4261.
15. Feinstein, D.L., Galea, E., Roberts, S., Berquist, H.W. & Reis, D.J. (1994) Induction of nitric oxide synthase in rat C6 gliana cells. J. Neurochem., 62, 315-321.
16. Fiebich, B.L., Butcher, R.D. & Gebicke-Haerter, P.J. (1998) Protein kinase C-mediated regulation of inducible nitric oxide synthase expression in cultured microglial cells. J. Immunol., 92, 170-178.
17. Galea, E., Feinstein, D.L. & Reis, D.J. (1992) Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc. Natl. Acad. Sci. USA, 89, 10945-10949.
18. Garća-Nogales, P., Almeida, A., Fernández, E., Medina, J.M. & Bolaños, J. (1999) Induction of glucose-6-phosphate dehydrogenase by lipopoly-saccharide contributes to preventing nitric oxide-mediated glutathione depletion in cultures rat astrocytes. J. Neurochem., 72, 1750-1758(1999).
19. Giulian, D. & Baker, T.J. (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci., 6, 2163-2178.
20. Graeber, M.B. & Kreutzberg, G.W. (1986) Astrocytes increase in glial fibrillary acidic protein during retrograde changes of facial motor neurons. J. Neurocytol., 15, 363-373.
21. Graeber, M.B. & Streit, W.J. (1990) Microglia: Immune network in the CNS. Brain Pathol., 1, 2-5.
22. Graeber, M.B., Tetzloff, W., Streit, W.J. & Kreutzberg, G.W. (1988) Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neurosci. Lett., 85, 317-321.
23. Haga, S., Akai, K. & Ishii, T. (1989) Demonstration of microglial cells in and around senile (neuritic) plaques in the Alzheimer brain. Acta Neuropathol., 77, 569-575.
24. Hailer, N.P., Wirjatijasa, F., Roser, N., Hischebeth, G.T., Korf, H.W. & Dehghani, F. (2001) Astrocytic factors protect neuronal integrity and reduce microglial activation in an in vitro model of N-methyl-D-aspartate-induced excitotoxic injury in organotypic hippocampal slice cultures. Eur. J. Neurosci., 14, 315-326.
25. Héry, C., Sébire, G., Peudenier, S. & Tardieu, M. (1995) Adhesion to human neurons and astrocytes of monocytes: The role of the interaction of CR3 and ICAM-1 and modulation by cytokines. J. Neuroimmunol., 57, 101-109.
26. Hewett, S.J., Corbett, J.A., McDaniel, M.L. & Choi, D.W. (1993) Interferon-γ and interleukin-1β induce nitric oxide formation from primary mouse astrocytes. Neurosci. Lett., 164, 229-232.
27. Hewett, J.A., Hewett, S.J., Winkler, S. & Pfeiffer, S.E. (1999) Inducible nitric oxide synthase expression in cultures enriched for mature oligodendrocytes is due to microglia. J. Neurosci. Res., 56, 189-198.
28. Jorgensen, M.B., Finsen, B.R., Jensen, M.B., Castellano, B., Diemer, N.H. & Zimmer, J. (1993) Microglial and astroglial reactions to ischemic and kainic acid-induced lesions to the adult rat hippocampus. Exp. Neurol., 120, 70-88.
29. Kong, L.Y., McMillian, M.K., Maronpot, R. & Hong, J.S. (1996) Protein tyrosine kinase inhibitors suppress the production of nitric oxide in mixed glia, microglia-enriched or astrocyte-enriched cultures. Brain Res., 729, 102-109.
30. Kyrkanides, S., Olschowka, J.A., Williams, J.P., Hansen, J.T. & O'Banion, M.K. (1999) TNF a and IL-1b mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury. J. Immunol., 95, 95-106.
31. Ledeboer, A., Brevé, J.J.P., Poole, S., Tilders, F.J.H. & Van Dam, A.-M. (2000) Interleukin-10, interleukin-4, and transforming growth factor-β differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia, 30, 134-142.
32. Lee, S.J. & Benveniste, E.N. (1999) Adhesion molecule expression and regulation on cells of the central nervous system. J. Neuroimmunol., 98, 77- 88.
33. Lee, S.C., Dickson, D.W., Brosnan, C.F. & Berman, J.W. (1993) Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J. Immunol., 150, 2659-2667.
34. Lee-Hall, L., Borke, R.C. & Anders, J.J. (1989) Transection or electrical stimulation of the hypoglossal nerve increases glial fibrillary acidic protein immunoreactivity in the hypoglossal nucleus. Brain Res., 490, 157-161.
35. Lieberman, A.P., Pitha, P.M., Shin, H.S. & Shin, M.L. (1989) Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc. Natl. Acad. Sci. USA, 86, 6348-6352.
36. Mahler, M., Ben-Ari, Y. & Represa, A. (1997) Differential expression of fibronectin, tenascin-C and NCAMs in cultured hippocampal astrocytes activated by kainate, bacterial lipopolysaccharide or basic fibroblast growth factor. Brain Res., 775, 63-73.
37. Meda, L., Cassatella, M.A., Szendrei, G.I., Otvos, L. Jr, Baron, P., Villalba, M., Ferrari, D. & Rossi, F. (1995) Activation of microglial cells by β-amyloid protein and interferon-γ. Nature, 374, 647-650.
38. Merrill, J.E., Ignaro, L.J., Sherman, M.P., Melinek, J. & Lane, T.E. (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol., 151, 2132-2141.
39. Merrill, J.E., Murphy, S.P., Mitrovic, B., Mackenzie-Graham, A., Dopp, J.C., Ding, M., Griscavage, J., Ignarro, L.J. & Lowenstein, C.J. (1997) Inducible nitric oxide synthase and nitric oxide production by oligodendrocytes. J. Neurosci. Res., 48, 372-384.
40. Pahan, K., Namboodiri, A.M.S., Sheikh, F.K., Smith, B.T. & Singh, I. (1997) Increasing cAMP attenuates induction of inducible nitric-oxide synthase in rat primary astrocytes. J. Biol. Chem., 272, 7786-7791.
41. Pang, Y., Cai, Z. & Rhodes, P.G. (2001) Analysis of genes differentially expressed in astrocytes stimulated with lipopolysaccharide using cDNA arrays. Brain Res., 914, 15-22.
42. Park, S.K. & Murphy, S. (1994) Duration of expression of inducible nitric oxide synthase in glial cells. J. Neurosci. Res., 39, 405-411.
43. Possel, H., Noack, H., Putzke, J., Wolf, G. & Sies, H. (2000) Selective upregulation of inducible nitric oxide synthase (iNOS) by lipopolysaccharide (LPS) and cytokines in microglia: In vitro and in vivo studies. Glia, 32, 51-59.
44. Raivich, G., Bohatschek, M., Kloss, C.U.A., 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.
45. Rischke, R. & Krieglstein, J. (1991) Postischemic neuronal damage causes astroglial activation and increase in local cerebral glucose utilization of rat hippocampus. J. Cereb. Blood Flow Metab., 11, 106-113.
46. Romero, L.I., Tatro, J.B., Field, J.A. & Reichlin, S. (1996) Roles of IL-1 and TNF-α in endotoxin-induced activation of nitric oxide synthase in cultured rat brain cells. Am. J. Physiol., 270, R326-R332.
47. Rosenman, S.J., Shrikant, P., Dubb, L., Benveniste, E.N. & Ransohoff, R.M. (1995) Cytokine-induced expression of vascular cell adhesion molecule-1 (VCAM-1) by astrocytes and astrocytoma cell lines. J. Immunol., 154, 1888-1899.
48. Shrikant, P., Chung, I.L., Ballestas, M.E. & Benveniste, E.N. (1994) Regulation of intercellular adhesion molecule-1 gene expression by tumor necrosis factor α, interleukin-1β, and interferon-γ in astrocytes. J. Neuroimmunol., 51, 209-220.
49. Simmons, M.L. & Murphy, S. (1992) Induction of nitric oxide synthase in glial cells. J. Neurochem., 59, 897-905.
50. Streit, W.J., Walter, S.A. & Pennell, N.A. (1999) Reactive microgliosis. Prog. Neurobiol., 57, 563-581.
51. Suk, K., Lee, J., Hur, J., Kim, Y.S., Lee, M.S., Cha, S.H., Kim, S.Y. & Kim, H. (2001) Activation-induced cell death of rat astrocytes. Brain Res., 900, 342- 347.
52. Tanaka, J. & Maeda, N. (1996) Microglial ramification requires nondiffusible factors derived from astrocytes. Exp. Neurol., 137, 367-375.
53. Tanaka, J., Toku, K., Matsuda, S., Sudo, S., Fujita, H., Sakanaka, M. & Maeda, N. (1998) Induction of resting microglia in culture medium devoid of glycine and serine. Glia, 24, 198-215.
54. Tanaka, J., Toku, K., Sakanaka, M. & Maeda, N. (1999) Morphological differentiation of microglial cells in culture: Involvement of insoluble factors derived from astrocytes. Neurosci. Res., 34, 207-215.
55. Vincent, V.A.M., Tilders, F.J.H. & Van Dam, A.-M. (1997) Inhibition of endotoxin-induced nitric oxide synthase production in microglial cells by the presence of astroglial cells: A role for transforming growth factor β. Glia, 19, 190-198.
56. Vincent, V.A.M., Van Dam, A.-M., Persoons, J.H.A., Schotanus, K., Steinbusch, H.W.N., Schoffelmeer, A.N.M. & Berkenbosch, F. (1996) Gradual inhibition of inducible nitric oxide synthase but not interleukin-1β production in rat microglial cells of endotoxin-treated mixed glial cell cultures. Glia, 17, 94-102.
57. Vitkovic, L., Bockaert, J. & Jacque, C. (2000) 'Inflammatory' cytokines: Neuromodulators in normal brain? J. Neurochem., 74, 457-471.
58. Yang, L., Tanaka, J., Zhang, B., Sakanaka, M. & Maeda, N. (1998) Astrocytes modulate nitric oxide production by microglial cells through secretion of serine and glycine. Biochem. Biophys. Res. Commun., 251, 277-282.
59. Zielasek, J., Tausch, M., Toyka, K.V. & Hartung, H.P. (1992) Production of nitrite by neonatal rat microglial cells/brain macrophages. Cell. Immunol., 141, 111-120.