Microglia are more susceptible than macrophages to apoptosis in the central nervous system in experimental autoimmune encephalomyelitis through a mechanism not involving Fas (CD95)

International Immunology

Volumn 10, Issue 7, 1998, Pages 935-941

  White, Catherine A ^a   McCombe, Pamela A ^a   Pender, Michael P ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Apoptosis; Experimental autoimmune encephalomyelitis; Fas (CD95); Macrophage; Microglia

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; FAS ANTIGEN; FAS LIGAND; FREUND ADJUVANT; GLYCOPROTEIN P 15095; MYELIN BASIC PROTEIN; PROTEIN BCL 2;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; DNA CONTENT; FEMALE; FLOW CYTOMETRY; INFLAMMATORY CELL; MACROPHAGE; MICROGLIA; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; RAT; SPINAL CORD;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FAS LIGAND PROTEIN; FEMALE; GUINEA PIGS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICROGLIA; PHENOTYPE; RATS; RATS, INBRED LEW; T-LYMPHOCYTES;

EID: 0031815933     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/10.7.935     Document Type: Article

References (48)

1. Pender, M. P., Nguyen, K. B., McCombe, P. A. and Kerr, J. F. 1991. Apoptosis in the nervous system in experimental allergic encephalomyelitis. J. Neurol. Sci. 104:81.
2. Pender, M. P., McCombe, P. A., Yoong, G. and Nguyen, K. B. 1992. Apoptosis of αβ; T lymphocytes in the nervous system in experimental autoimmune encephalomyelitis: its possible implications for recovery and acquired tolerance. J. Autoimmun. 5:401.
3. Schmied, M., Breitschopf, H., Gold, R., Zischler, H., Rothe, G., Wekerle, H. and Lassmann, H. 1993. Apoptosis of T lymphocytes in experimental autoimmune encephalomyelitis. Evidence for programmed cell death as a mechanism to control inflammation in the brain. Am. J. Pathol. 143:446.
4. Pender, M. P. 1995. Experimental autoimmune encephalomyelitis. In Pender, M. P. and McCombe, P. A., ed., Autoimmune Neurological Disease, p. 26. Cambridge University Press. Cambridge.
5. Kennedy, M. K., Torrance, D. S., Picha, K. S. and Mohler, K. M. 1992. Analysis of cytokine mRNA expression in the central nervous system of mice with experimental autoimmune encephalomyelitis reveals that IL-10 mRNA expression correlates with recovery. J. Immunol. 149:2496.
6. Huitinga, I., van Rooijen, N., de Groot, C. J., Uitdehaag, B. M. and Dijkstra, C. D. 1990 Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 172:1025.
7. Hinrichs, D. J., Wegmann, K. W. and Dietsch, G. N. 1987. Transfer of experimental allergic encephalomyelitis to bone marrow chimeras. Endothelial cells are not a restricting element. J. Exp. Med. 166:1906.
8. Hickey, W. F., Kimura, H., Hinrichs, D. J., Wegmann, K. W., Dietsch, G. N., Myers, K. J., Dougherty, J. P. and Ron, Y. 1988. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290.
9. Myers, K. J., Dougherty, J. P. and Ron, Y. 1993. In vivo antigen presentation by both brain parenchymal cells and hematopoietically derived cells during the induction of experimental autoimmune encephalomyelitis. J. Immunol. 151:2252.
10. Matsumoto, Y., Hara, N., Tanaka, R. and Fujiwara, M. 1986. Immunohistochemical analysis of the rat central nervous system during experimental allergic encephalomyelitis, with special reference to la-positive cells with dendritic morphology. J. Immunol. 136:3668.
11. McCombe, P. A., Fordyce, B. W., de Jersey, J., Yoong, G. and Pender, M. P. 1992. Expression of CD45RC and la antigen in the spinal cord in acute experimental allergic encephalomyelitis: an immunocytochemical and flow cytometric study. J. Neurol. Sci. 113:177.
12. McCombe, P. A., de Jersey, J. and Pender, M. P. 1994. Inflammatory cells, microglia and MHC class II antigen-positive cells in the spinal cord of Lewis rats with acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 51:153.
13. Ford, A. L., Foulcher, E., Lemckert, F. A. and Sedgwick, J. D. 1996. Microglia induce CD4 T lymphocyte final effector function and death. J. Exp. Med. 184:1737.
14. + encephalitogenic T cells. Eur. J. Immunol. 24:2609.
15. Tabi, Z., McCombe, P. A. and Pender, M. P. 1995. Antigen-specific down-regulation of myelin basic protein-reactive T cells during spontaneous recovery from experimental autoimmune encephalomyelitis: further evidence of apoptotic deletion of autoreactive T cells in the central nervous system. Int. Immunol. 7:967.
16. + T lymphocytes in the spinal cord during recovery from experimental autoimmune encephalomyelitis induced in Lewis rats by inoculation with myelin basic protein. J. Neurol. Sci. 139:1.
17. White, C. A., McCombe, P. A. and Pender, M. P. 1998. The roles of Fas, Fas ligand and Bcl-2 in T cell apoptosis in the central nervous system in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 82:47.
18. Nguyen, K. B., McCombe, P. A. and Pender, M. P. 1997. Increased apoptosis of T lymphocytes and macrophages in the central and peripheral nervous systems of Lewis rats with experimental autoimmune encephalomyelitis treated with dexamethasone. J. Neuropathol. Exp. Neurol. 56:58.
19. Nguyen, K. B., McCombe, P. A. and Pender, M. P. 1994. Macrophage apoptosis in the central nervous system in experimental autoimmune encephalomyelitis. J. Autoimmun. 7:145.
20. + lymphocytes delete activated macrophages through the Fas/APO-1 antigen pathway. Proc. Natl Acad. Sci. USA 92:11225.
21. Deibler, G. E., Martenson, R. E. and Kies, M. W. 1972. Large scale preparation of myelin basic protein from central nervous tissue of several mammalian species. Prep. Biochem. 2:139.
22. Pender, M. P. 1986. Ascending impairment of nociception in rats with experimental allergic encephalomyelitis. J. Neurol. Sci. 75:317.
23. Torres-Nagel, N. E., Gold, D. P. and Hünig, T. 1993. Identification of rat TCR β-V8.2, 8.5, and 10 gene products by monoclonal antibodies. Immunogenetics 37:305
24. Sedgwick, J. D., Schwender, S., Imrich, H., Dorries, R., Butcher, G. W. and ter Meulen, V. 1991. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc. Natl Acad. Sci. USA 88:7438.
25. + T cells compared. J. Immunol. 154:4309.
26. Carbonari, M., Cibati, M., Cherchi, M., Sbarigia, D., Pesce, A. M., Dell'Anna, L., Modica, A. and Fiorilli, M. 1994. Detection and characterization of apoptotic peripheral blood lymphocytes in human immunodeficiency virus infection and cancer chemotherapy by a novel flow immunocytometric method. Blood 83:1268.
27. Gehrmann, J. and Banati, R. B. 1995. Microglial turnover in the injured CNS: activated microglia undergo delayed DNA fragmentation following peripheral nerve injury. J. Neuropathol. Exp. Neurol 54:680.
28. Albina, J. E., Cui, S., Mateo, R. B. and Reichner, J. S. 1993. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150:5080.
29. Brune, B., Golkel, C. and von Knethen, A. 1996. Cytokine and low-level nitric oxide prestimulation block p53 accumulation and apoptosis of RAW 264.7 macrophages. Biochem. Biophys. Res. Commun. 229:396.
30. Mitrovic, B., Ignarro, L. J., Montestruque, S., Smoll, A. and Merrill, J, E. 1994. Nitric oxide as a potential pathological mechanism in demyelination: its differential effects on primary glial cells in vitro. Neuroscience 61:575.
31. Mitrovic, B., Ignarro, L. J., Vinters, H. V., Akers, M. A., Schmid, I., Uittenbogaart, C. and Merrill, J. E. 1995. Nitric oxide induces necrotic but not apoptotic cell death in oligodendrocytes. Neuroscience 65:531.
32. Mangan, D. F., Robertson, B. and Wahl, S. M. 1992. IL-4 enhances programmed cell death (apoptosis) in stimulated human monocytes. J. Immunol. 148:1812.
33. Oritani, K., Kaisho, T., Nakajima, K. and Hirano, T. 1992. Retinoic acid inhibits interleukin-6-induced macrophage differentiation and apoptosis in a murine hematopoietic cell line, Y6. Blood 80:2298.
34. Xiao, B. G., Bai, X. F., Zhang, G. X. and Link, H. 1997. Transforming growth factor beta 1 induces apoptosis of rat microglia without relation to bcl 2 oncoprotein expression. Neurosci. Lett. 226:71.
35. Merrill, J. E., Kono, D. H., Clayton, J., Ando, D. G., Hinton, D. R. and Hofman, F. M. 1992. Inflammatory leukocytes and cytokines in the peptide-induced disease of experimental allergic encephalomyelitis in SJL and B10.PL mice. Proc. Natl Acad. Sci. USA 89:574.
36. Malipiero, U. V., Frei, K. and Fontana, A. 1990. Production of hemopoietic colony-stimulating factors by astrocytes. J. Immunol. 144:3816.
37. Mangan, D. F. and Wahl, S. M. 1991. Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines. J, Immunol. 147:3408.
38. Tomozawa, Y., Inoue, T., Takahashi, M., Adachi, M. and Satoh, M. 1996. Apoptosis of cultured microglia by the deprivation of macrophage colony-stimulating factor. Neurosci. Res. 25:7.
39. Suttles, J., Evans, M., Miller, R. W., Poe, J. C., Stout, R. D. and Wahl, L. M. 1996. T cell rescue of monocytes from apoptosis: role of the CD40-CD40L interaction and requirement for CD40-mediated induction of protein tyrosine kinase activity. J. Leuk. Biol. 60:651.
40. Ohmori, K., Hong, Y., Fujiwara, M. and Matsumoto, Y. 1992. In situ demonstration of proliferating cells in the rat central nervous system during experimental autoimmune encephalomyelitis. Evidence suggesting that most infiltrating T cells do not proliferate in the target organ Lab. Invest. 66:54.
41. Matsumoto, Y., Ohmori, K. and Fujiwara, M. 1992. Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J. Neuroimmunol. 37:23.
42. Gehrmann, J., Matsumoto, Y. and Kreutzberg, G. W. 1995. Microglia: intrinsic immuneffector cell of the brain. Brain Res Rev. 20:269.
43. Reid, D. M., Perry, V. H., Andersson, P. B. and Gordon, S. 1993. Mitosis and apoptosis of microglia in vivo induced by an anti-CR3 antibody which crosses the blood-brain barrier. Neuroscience 56:529.
44. Bellingan, G. J., Caldwell, H., Howie, S. E., Dransfield, I. and Haslett, C. 1996. In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J. Immunol. 157:2577.
45. Sabelko, K. A., Kelly, K. A., Nahm, M. H., Cross, A. H. and Russell, J. H. 1997. Fas and Fas ligand enhance the pathogenesis of experimental allergic encephalomyelitis, but are not essential for immune privilege in the central nervous system. J. Immunol 159:3096.
46. Waldner, H., Sobel, R. A., Howard, E. and Kuchroc, V. K. 1997. Fas and FasL deficient mice are resistant to induction of autoimmune encephalomyelitis. J. Immunol. 159:3100.
47. Bellgrau, D., Gold, D., Selawry, H., Moore, J., Franzusoff, A. and Duke, R. C. 1995. A role for CD95 ligand in preventing graft rejection. Nature 377:630.
48. Griffith, T. S., Brunner, T., Fletcher, S. M., Green, D. R. and Ferguson, T. A. 1995. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 270:1189.