Soluble factors released by Toxoplasma gondii-infected astrocytes down-modulate nitric oxide production by gamma interferon-activated microglia and prevent neuronal degeneration

Infection and Immunity

Volumn 71, Issue 4, 2003, Pages 2047-2057

  Rozenfeld, Claudia ^a   Martinez, Rodrigo ^a   Figueiredo, Rodrigo T ^a   Bozza, Marcelo T ^a   Lima, Flávia R S ^a   Pires, Ana Lúcia ^c   Silva, Patrícia M ^c   Bonomo, Adriana ^b   Vieira, Joseli ^c   De Souza, Wanderley ^a   Moura Neto, Vivaldo ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE ACTIVATOR; ANTIBODY; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; FORSKOLIN; GAMMA INTERFERON; INTERLEUKIN 10 ANTIBODY; NITRIC OXIDE; PROSTAGLANDIN E2;

ANIMAL CELL; ARTICLE; ASTROCYTE; AUTOCRINE EFFECT; CONTROLLED STUDY; IMMUNE RESPONSE; MICROGLIA; MOUSE; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; ASTROCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYCLIC AMP; DINOPROSTONE; DOWN-REGULATION; INTERFERON TYPE II; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; MICROGLIA; NEURONS; NITRIC OXIDE; SOLUBILITY; TOXOPLASMA;

EID: 0344405677     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.4.2047-2057.2003     Document Type: Article

References (73)

1. Aloisi, F. 1999. The role of microglia and astrocytes in CNS immune surveillance and immunopathology. Adv. Exp. Med. Biol. 468:123-133.
2. Aloisi, F., E. Ambrosini, S. Columba-Cabezas, R. Magliozzi, and B. Serafini. 2001. Intracerebral regulation of immune responses. Ann. Med. 33:510-515.
3. Aloisi, F., G. Penna, J. Cerase, B. Menendez Iglesias, and L. Adorini. 1997. IL-12 production by central nervous system microglia is inhibited by astrocytes. J. Immunol. 159:1604-1612.
4. Aloisi, F., R. De Simone, S. Columba-Cabezas, and G. Levi. 1999. Opposite effects of interferon-gamma and prostaglandin E2 on tumor necrosis factor and interleukin-10 production in microglia: a regulatory loop controlling microglia pro- and anti-inflammatory activities. J. Neurosci. Res. 56:571-580.
5. Bachis, A., A. M. Colangelo, S. Vicini, P. P. Doe, M. A. De Bernardi, G. Brooker, and I. Mocchetti. 2001. Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J. Neurosci. 21:3104-3112.
6. Bohne, W., J. Heesemann, and U. Gross. 1994. Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infect. Immun. 62:1761-1767.
7. Bolanos, J. P., P. Garcia-Nogales, V. Vega-Agapito, M. Delgado-Esteban, P. Cidad, and A. Almeida. 2001. Nitric oxide-mediated mitochondrial impairment in neural cells: a role for glucose metabolism in neuroprotection. Prog. Brain Res. 132:441-454.
8. Brewer, K. L., J. R. Bethea, and R. P. Yezierski. 1999. Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp. Neurol. 159:484-493.
9. Burke, J. M., C. W. Roberts, C. A. Hunter, M. Murray, and J. Alexander. 1994. Temporal differences in the expression of mRNA for IL-10 and IFN-gamma in the brains and spleens of C57BL/10 mice infected with Toxoplasma gondii. Parasite Immunol. 16:305-314.
10. Caggiano, A. O., and R. P. Kraig. 1999. Prostaglandin E receptor subtypes in cultured rat microglia and their role in reducing lipopolysaccharide-induced interleukin-1β production. J. Neurochem. 72:565-575.
11. Carlson, N. G., W. A. Wieggel, J. Chen, A. Bacchi, S. W. Rogers, and L. C. Gahring. 1999. Inflammatory cytokines IL-1 alpha, IL-1 beta, IL-6, and TNF-alpha impart neuroprotection to an excitotoxin through distinct pathways. J. Immunol. 163:3963-3968.
12. Channon, J. Y., and L. H. Kasper. 1996. Toxoplasma gondii-induced immune suppression by human peripheral blood monocytes: role of gamma interferon. Infect. Immun. 64:1181-1189.
13. Chao, C. C., G. Gekker, S. Hu, and P. K. Peterson. 1994. Human microglial cell defence against Toxoplasma gondii. J. Immunol. 152:1246-1252.
14. Chao, C. C., S. Hu, and P. K. Peterson. 1995. Cytokines and neurotoxicity. Crit. Rev. Neurobiol. 9:189-205.
15. Chao, C. C., S. Hu, T. W. Molitor, E. G. Shaskan, and P. K. Peterson. 1992. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 149:2736-2741.
16. Chuenkova, M. V., and M. A. Pereira. 2001. The T cruzi trans-sialidase induces PC12 cell differentiation via MAPK/ERK pathway. Neuroreport 12:3715-3718.
17. Chuenkova, M. V., and M. A. Pereira. 2000. A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Mol. Biol. Cell 11:1487-1498.
18. 2. AIDS 9:441-445.
19. Ding, A. H., C. F. Nathan, and D. J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
20. DiProspero, N. A., S. Meiners, and H. M. Geller. 1997. Inflammatory cytokines interact to modulate extracellular matrix and astrocytic support of neurite outgrowth. Exp. Neurol. 148:628-639.
21. Fischer, H. G., B. Ntzgen, G. Relchmann, and U. Hadding. 1997. Cytokine responses induced by Toxoplasma gondii in astrocytes and microglial cells. Eur. J. Immunol. 27:1539-1548.
22. Fretland, D. J. 1992. Potential role of prostaglandins and leukotrienes in multiple sclerosis and experimental allergic encephalomyelitis. Prostaglandins Leukot. Essent. Fatty Acids 45:249-257.
23. Freund, Y. R., N. T. Zaveri, and H. S. Javitz. 2001. In vitro investigation of host resistance to Toxoplasma gondii infection in microglia of BALB/c and CBA/Ca mice. Infect. Immun. 69:765-772.
24. Gazzinelli, R. T., F. T. Hakim, S. Hieny, G. M. Shearer, and A. Sher. 1991. Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J. Immunol. 146:286-292.
25. Gazzinelli, R. T., I. P. Oswald, S. L. James, and A. Sher. 1992. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J. Immunol. 148:1792-1796.
26. Gazzinelli, R. T., M. Wysocka, S. Hieny, T. Scharton-Kersten, A. Cheever, R. Kuhn, W. Muller, G. Trinchieri, and A. Sher. 1996. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J. Immunol. 157:798-805.
27. Giovannoni, G., S. J. Heales, J. M. Land, and E. J. Thompson. 1998. The potential role of nitric oxide in multiple sclerosis. Mult. Scler. 4:212-216.
28. Grilli, M., I. Barbieri, H. Basudev, R. Brusa, C. Casati, G. Lozza, and E. Ongini. 2000. Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur. J. Neurosci. 12:2265-2272.
29. Hailer, N. P., F. Wirjatijasa, N. Roser, G. T. Hischebeth, H. W. Korf, and F. Dehghani. 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.
30. Halonen, S. K., G. A. Taylor, and L. M. Weiss. 2001. Gamma interferon-induced inhibition of Toxoplasma gondii in astrocytes is mediated by IGTP. Infect. Immun. 69:5573-5576.
31. Helliwell, B. 2001. Role of free radicals in the neurodegenerative diseases. Drugs Aging 18:685-716.
32. 2 production from primary mouse astrocytes independent of nitric oxide formation. J. Neuroimmunol. 94:134-143.
33. Hofman, F. M., D. R. Hinton, K. Johnson, and J. E. Merrill. 1989. Tumor necrosis factor identified in multiple sclerosis brain. J. Exp. Med. 170:607-612.
34. Israelski, D. M., and J. S. Remington. 1993. Toxoplasmosis in non-AIDS immunocompromised host. Curr. Opin. Top. Infect. Dis. 13:322-356.
35. Jamra, L. M. F., and M. P. L. Vieira. 1991. Isolamento do Toxoplasma gondii de exsudato peritoneal e órgāos de camundongos corn infecção experimental. Rev. Inst. Med. Trop. São Paulo 33:435-441.
36. Jun, C. D., S. H. Kim, C. T. Soh, S. S. Kang, and H. T. Chung. 1993. Nitric oxide mediates the toxoplasmastatic activity of murine microglial cells in vitro. Immunol. Investig. 22:487-501.
37. Kammer, G. M. 1988. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol. Today 9:222-229.
38. Kang, H., and Y. Suzuki. 2001. Requirement of non-T cells that produce gamma interferon for prevention of reactivation of Toxoplasma gondii infection in the brain. Infect. Immun. 69:2920-2927.
39. Khan, I. A., J. D. Schwartzman, T. Matsuura, and L. H. Kasper. 1997. A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc. Natl. Acad. Sci. USA 94:13955-13960.
40. 1 protects cultured spinal neurons against the effects of nitric oxide toxicity. Neuropharmacology 42:714-723.
41. 2 on microglial functions. Biochimie 80:899-904.
42. Li, G., J. A. Harton, X. Zhu, and J. P. Ting. 2001. Downregulation of CIITA function by protein kinase A (PKA)-mediated phosphorylation: mechanism of prostaglandin E, cyclic AMP, and PKA inhibition of class II major histocompatibility complex expression in monocytic lines. Mol. Cell. Biol. 14:4626-4635.
43. Lima, F. S. L., A. Gervais, C. Colin, M. Izembart, V. Moura-Neto, and M. Mallat. 2001. Regulation of microglial development: a novel role for thyroid hormone. J. Neurosci. 21:2028-2038.
44. Luder, C. G., T. Lang, B. Beuerle, and U. Gross. 1998. Down-regulation of MHC class II molecules and inability to up-regulate class I molecules in murine macrophages after infection with Toxoplasma gondii. Clin. Exp. Immunol. 112:308-316.
45. Mattson, M. P., S. W. Barger, K. Furukawa, A. J. Bruce, T. Wyss-Coray, R. J. Mark, and L. Mucke. 1997. Cellular signaling roles of TGF beta, TNF alpha and beta APP in brain injury responses and Alzheimer's disease. Brain Res. Rev. 23:47-61.
46. McGeer, P. L., S. Itagaki, H. Akiyama, and E. G. McGeer. 1988. Rate of cell death in parkinsonism indicates active neuropathological process. Ann. Neurol. 24:574-576.
47. McMillian, M., L. Y. Kong, S. M. Sawin, B. Wilson, K. Das, P. Hudson, J. S. Hong, and G. Bing. 1995. Selective killing of cholinergic neurons by microglial activation in basal forebrain mixed neuronal/glial cultures. Biochem. Biophys. Res. Commun. 215:572-577.
48. Merrill, J. E. 1992. Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Dev. Neurosci. 14:1-10.
49. Minghetti, L., A. Nicolini, E. Polazzi, C. Creminon, J. Maclouf, and G. Levi. 1997. Prostaglandin E2 downregulates inducible nitric oxide synthase expression in microglia by increasing cAMP levels. Adv. Exp. Med. Biol. 433:181-184.
50. 2 and by cyclooxygenase inhibitors. Glia 19:152-160.
51. Minghetti, L., E. Polazzi, A. Nicolini, and G. Levi. 1998. Opposite regulation of prostaglandin E2 synthesis by transforming growth factor-beta 1 and interleukin 10 in activated microglial cultures. J. Neuroimmunol. 82:31-39.
52. Penkowa, M., T. Moos, J. Carrasco, H. Hadberg, A. Molinero, H. Bluethmann, and J. Hidalgo. 1999. Strongly compromised inflammatory response to brain injury in interleukin-6-deficient mice. Glia 25:343-357.
53. Phipps, R. P., S. H. Stein, and R. L. Roper. 1991. A new view of prostaglandin E regulation of the immune response. Immunol. Today 12:349-352.
54. Rogers, J., J. Luber-Narod, S. D. Styren, and W. H. Civin. 1988. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology, of Alzheimer's disease. Neurobiol. Aging 9:339-349.
55. Rostasy, K., L. Monti, C. Yiannoutsos, M. Kneissl, J. Bell, T. L. Kemper, J. C. Hedreen, and B. A. Navia. 1999. Human immunodeficiency virus infection, inducible nitric oxide synthase expression, and microglial activation: pathogenic relationship to the acquired immunodeficiency syndrome dementia complex. Ann. Neurol. 46:207-216.
56. Scharton-Kersten, T. M., G. Yap, J. Magram, and A. Sher. 1997. Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185:1261-1273.
57. Schluter, D., M. Deckert-Schluter, E. Lorenz, T. Meyer, M. Rollinghoff, and C. Bogdan. 1999. Inhibition of inducible nitric oxide synthase exacerbates chronic cerebral toxoplasmosis in Toxoplasma gondii-susceptible C57BL/6 mice but does not reactivate the latent disease in T. gondii-resistant BALB/c mice. J. Immunol. 162:3512-3518.
58. Schluter, D., N. Kaefer, H. Hof, O. D. Wiestler, and M. Deckert-Schluter. 1997. Expression pattern and cellular origin of cytokines in the normal and Toxoplasma gondii-infected murine brain. Am. J. Pathol. 150:1021-1035.
59. Silva, N. M., W. L. Tafuri, J. I. Alvarez-Leite, J. R. Mineo, and R. T. Gazzinelli. 2002. Toxoplasma gondii: in vivo expression of BAG-5 and cyst formation is independent of TNF p55 receptor and inducible nitric oxide synthase functions. Microbes Infect. 4:261-270.
60. Stoll, G., S. Jander, and M. Schroeter. 2000. Cytokines in CNS disorders: neurotoxicity versus neuroprotection. J. Neural Transm. 59:81-89.
61. Suzuki, Y. 1999. Genes, cells and cytokines in resistance against development of toxoplasmic encephalitis. Immunobiology 201:255-271.
62. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
63. Suzuki, Y., H. Kang, S. Parmley, S. Lim, and D. Park. 2000. Induction of tumor necrosis factor-alpha and inducible nitric oxide synthase fails to prevent toxoplasmic encephalitis in the absence of interferon-gamma in genetically resistant BALB/c mice. Microbes Infect. 2:455-462.
64. Tenter, A. M., A. R. Heckeroth, and L. M. Weiss. 2000. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30:1217-1258.
65. 2 and a β-adrenergic agonist. Glia 11:383-386.
66. Trentin, A. G., M. Alvarez-Silva, and V. Moura-Neto. 2001. Thyroid hormone induces cerebellar astrocytes and C6 glioma cells to secrete mitogenic growth factors. Am. J. Physiol. Endocrinol. Metab. 281:1088-1094.
67. Tsacopoulos, M., and P. J. Magistretti. 1996. Metabolic coupling between glia and neurons. J. Neurosci. 16:877-885.
68. Vane, J. R. 2002. Back to an aspirin a day? Science 296:474-475.
69. Villegas, E. N., U. Wille, L. Craig, P. S. Linsley, D. M. Rennick, R. Peach, and C. A. Hunter. 2000. Blockade of costimulation prevents infection-induced immunopathology in interleukin-10-deficient mice. Infect. Immun. 68:2837-2844.
70. Wille, U., E. N. Villegas, B. Striepen, D. S. Roos, and C. A. Hunter. 2001. Interleukin-10 does not contribute to the pathogenesis of a virulent strain of Toxoplasma gondii. Parasite Immunol. 23:291-296.
71. Yap, G. S., and A. Sher. 1999. Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-gamma- and tumour necrosis factor (TNF)-alpha-dependent host resistance to the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 189:1083-1092.
72. 2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J. Neurochem. 76:855-864.
73. Zhang, S. C., B. D. Goetz, J. L. Carre, and I. D. Duncan. 2001. Reactive microglia in dysmyelination and demyelination. Glia 34:101-109.