Targeted expression of baculovirus p35 caspase inhibitor in oligodendrocytes protects mice against autoimmune-mediated demyelination

EMBO Journal

Volumn 19, Issue 3, 2000, Pages 341-348

  Hisahara, Shin ^a   Araki, Takashi ^b   Sugiyama, Fumihiro ^c   Yagami, Ken Ichi ^c   Suzuki, Misao ^d   Abe, Kuniya ^e   Yamamura, Ken Ichi ^d,e   Miyazaki, Jun Ichi ^f   Momoi, Takashi ^g   Saruta, Takao ^b   Bernard, Claude C A ⁱ   Okano, Hideyuki ^a,h   Miura, Masayuki ^a,h  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d KUMAMOTO UNIVERSITY   (Japan)

^e KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

^f OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^g NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^h JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

ⁱ LA TROBE UNIVERSITY   (Australia)

Author keywords

Apoptosis; Baculovirus p35; Caspase; Demyelination; Oligodendrocyte

Indexed keywords

CASPASE INHIBITOR; MYELIN ASSOCIATED GLYCOPROTEIN; PROTEIN P35;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNITY; BACULOVIRUS; CONTROLLED STUDY; DEMYELINATION; IMMUNIZATION; MACROGLIA; MACROPHAGE; MOUSE; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS; RODENTIA; UNIDENTIFIED BACULOVIRUS;

EID: 0034142394     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.3.341     Document Type: Article

References (54)

1. Bauer,J., Berkenbosch,F., Van Dam,A.M. and Dijkstra,C.D. (1993) Demonstration of interleukin-1β in Lewis rat brain during experimental allergic encephalomyelitis by immunocytochemistry at the light and ultrastructural level. J. Neuroimmunol., 48, 13-21.
2. Beidler,D.R., Tewari,M., Friesen,P.D., Poirier,G. and Dixit,V.M. (1995) The baculovirus p35 protein inhibits Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem., 270, 16526-16528.
3. Blasi,F. et al. (1999) Constitutive expression of interleukin-1β (IL-1β) in rat oligodendrocytes. Biol. Chem., 380, 259-264.
4. Bump,N.J. et al. (1995) Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science, 269, 1885-1888.
5. Cerretti,D.P. et al. (1992) Molecular cloning of the interleukin-1β converting enzyme. Science, 256, 97-100.
6. Chin,Y.E., Kitagawa,M., Kuida,K., Flavell,R.A. and Fu,X.Y. (1997) Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol., 17, 5328-5337.
7. Darmon,A.J., Nicholson,D.W. and Bleackley,R.C. (1995) Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature, 377, 446-448.
8. Dowling,P., Husar,W., Menonna,J., Donnenfeld,H., Cook,S. and Sidhu,M. (1997) Cell death and birth in multiple sclerosis brain. J. Neurol Sci., 149, 1-11.
9. D'Souza,S., Alinauskas,K., McCrea,E., Goodyer,C. and Antel,J.P. (1995) Differential susceptibility of human CNS-derived cell populations to TNF-dependent and independent immune-mediated injury. J. Neurosci., 15, 7293-7300.
10. D'Souza,S.D., Bonetti,B., Balasingam,V., Cashman,N.R., Barker,P.A., Troutt,A.B., Raine,C.S. and Antel,J.P. (1996) Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J. Exp. Med., 184, 2361-2370.
11. Ghayur,T. et al. (1997) Caspase-1 processes IFN-γ-inducing factor and regulates LPS-induced IFN-γ production. Nature, 386, 619-623.
12. Gold,R., Hartung,H.P. and Lassmann,H. (1997) T-cell apoptosis in autoimmune diseases: termination of inflammation in the nervous system and other sites with specialized immune-defense mechanisms. Trends Neurosci., 20, 399-404.
13. Gow,A., Friedrich,V.L.,Jr and Lazzarini,R.A. (1992) Myelin basic protein gene contains separate enhancers for oligodendrocytes and Schwann cell expression. J. Cell Biol., 119, 605-616.
14. Gu,Y. et al (1997) Activation of interferon-γ inducing factor mediated by interleukin-1β converting enzyme. Science, 275, 206-209.
15. Hali,A., Giese,N.A. and Richardson,W.D. (1996) Spinal cord oligodendrocytcs develop from ventrally derived progenitor cells that express PDGFα-receptors. Development, 122, 4085-4094.
16. Hirota,H., Chen,J., Betz,U.A., Rajewsky,K., Gu,Y., Ross,J.Jr, Muller,W. and Chien,K.R. (1999) Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress. Cell, 97, 189-198.
17. Hisahara,S., Shoji,S., Okano,H. and Miura,M. (1997) ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J. Neurochem., 69, 10-20.
18. Izquierdo,M, Grandien,A., Criado,L.M., Robles,S., Leonardo,E., Albar,J.P., de Buitrago,G.G. and Martinez,A.C. (1999) Blocked negative selection of developing T cells in mice expressing the baculovirus p35 caspase inhibitor. EMBO J., 18, 156-166.
19. Kagawa,T. et al. (1994) Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron. 13, 427-442.
20. Kanegae,Y., Lee,G., Sato,Y., Tanaka,M., Nakai,M., Sakaki,T., Sugano,S. and Saito,I. (1995) Efficient gene activation in mammalian cells by-using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acids Res., 23, 3816-3821.
21. Kimura,M., Sato,M., Akatsuka,A., Nozawa-Kimura,S., Takahashi,R., Yokoyama,M., Nomura,T. and Katsuki,M. (1989) Restoration of myelin formation by a single type of myelin basic protein in transgenic shiverer mice. Proc. Natl Acad. Sci. USA, 86, 5661-5665.
22. Kouroku,Y., Urase,K., Fujita,E., Isahara,K., Ohsawa,Y., Uchiyama,Y., Momoi,M.Y. and Momoi,T. (1998) Detection of activated caspase-3 by a cleavage site-directed antiserum during naturally occurring DRG neurons apoptosis. Biochem. Biophys. Res. Commun., 247, 780-784.
23. Kulkarni,R.N., Bruning,J.C., Winnay,J.N., Postic,C., Magnuson,M.A. and Kahn,C.R. (1999) Tissue-specific knockout of the insulin receptor in pancreatic β cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell, 96, 329-339.
24. Laird,P.W., Zijderveld,A., Linders,K., Rudnicki,M.A., Jaenisch,R. and Berns,A. (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res., 19, 4293.
25. Ledeen,R.W. and Chakraborty,G. (1998) Cytokines, signal transduction and inflammatory demyelination: review and hypothesis. Neurochem. Res., 23, 277-289.
26. Lee,S.C. and Raine,C.S. (1989) Multiple sclerosis: oligodendrocytes in active lesions do not express class II major histocompatibility complex molecules. J. Neuroimmunol., 25, 261-266.
27. Li,H., Zhu,H., Xu,C.J. and Yuan,J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94, 491-501.
28. Liu,J., Marino,M.W., Wong,G., Grail,D., Dunn,A., Bettadapura,J., Slavin,A.J., Old,L. and Bernard,C.C. (1998) TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nature Med., 4, 78-83.
29. Los,M., Wesselborg,S. and Schulze-Osthoff,K. (1999) The role of caspases in development, immunity and apoptotic signal transduction: lessons from knockout mice. Immunity, 10, 629-639.
30. Louis,J.C. Magal,E., Takayama,S. and Varon,S. (1993) CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science, 259, 689-692.
31. Luo,X., Budihardjo,L. Zou,H., Slaughter,C. and Wang,X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94, 481-190.
32. Malipiero,U., Frei,K., Spanaus,K.S., Agresti,C, Lassmann,H., Hahne,M., Tschopp,J., Eugster,H.P. and Fontana,A. (1997) Myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis is chronic/relapsing in perform knockout mice, but monophasic in Fas- and Fas ligand-deficient lpr and gld mice. Eur. J. Immunol., 27, 3151-3160.
33. Miura,M., Tamura,T., Aoyama,A. and Mikoshiba,K. (1989) The promoter elements of the mouse myelin basic protein gene function efficiently in NG108-15 neuronal/glial cells. Gene, 75, 31-38.
34. Nagata,S. (1997) Apoptosis by death factor. Cell, 88, 355-365.
35. Okano,H., Aruga,J., Nakagawa,T., Shiota,C. and Mikoshiba,K. (1991) Myelin basic protein gene and the function of antisense RNA in its repression in myelin-deficient mutant mouse. J. Neurochem., 56, 560-567.
36. 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, 81-87.
37. Raine,C.S. (1997) The Norton Lecture: a review of the oligodendrocyte in the multiple sclerosis lesion. J. Neuroimmunol., 77, 135-152.
38. Ruddle,N.H., Bergman,C.M., McGrath,K.M., Lingenheld,E.G., Grunnet,M.L., Padula,S.J. and Clark,R.B. (1990) An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med., 172, 1193-1200.
39. Sakai,K. and Miyazaki,J. (1997) A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the ere transgene transmission. Biochem. Biophys. Res. Commun., 237, 318-324.
40. Sarin,A., Williams,M.S., Alexander-Miller,M.A., Berzofsky,J.A., Zacharchuk,C.M. and Henkart,P.A. (1997) Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity, 6, 209-215.
41. Scaffidi,C., Fulda,S., Srinivasan,A., Friesen,C., Li,F., Tomaselli,K.J., Debatin,K.M., Krammer,P.H. and Peter,M.E. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J., 17, 1675-1687.
42. Selmaj,K.W. and Raine,C.S. (1988) Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol., 23, 339-346.
43. Selmaj,K., Raine,C.S., Cannella,B. and Brosnan,C.F. (1991) Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest., 87, 949-954
44. Sharief,M.K. and Henlges,R. (1991) Association between tumor necrosis factor-α and disease progression in patients with multiple sclerosis. N. Engl. J. Med., 325, 467-472.
45. Simmons,R.D. and Willenborg,D.O. (1990) Direct injection of cytokines into the spinal cord causes autoimmune encephalomyelitis-like inflammation. J. Neurol. Sci., 100, 37-42.
46. Stoll,G., Muller,S., Schmidt,B., van der Meide,P., Jung,S., Toyka,K.V. and Hartung,H.P. (1993) Localization of interferon-γ and la-antigen in T cell line-mediated experimental autoimmune encephalomyelitis. Am. J. Pathol, 142, 1866-1875.
47. Strasser,A., Harris,A.W., Huang,D.C., Krammer,P.H. and Cory,S. (1995) Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J., 14, 6136-6147.
48. Tansey,F.A. and Cammer,W. (1991) A [pi] form of glutathione-S-transferase is a myelin- and oligodendrocyte-associated enzyme in mouse brain. J. Neurochem., 57, 95-102.
49. Thornberry,N.A. et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature, 356, 768-774.
50. Trapani,J.A., Jans,D.A., Jans,P.J., Smyth,M.J., Browne,K.A. and Sutton,V.R. (1998) Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perform are caspase-dependent, but cell death is caspase-independent. J. Biol. Chem., 273, 27934-27938.
51. Tsien,J.Z., Chen,D.F, Gerber,D., Tom,C., Mercer,E.H., Anderson,D.J., Mayford,M., Kandel,E.R. and Tonegawa,S. (1996) Subregion- and cell type-restricted gene knockout in mouse brain. Cell, 87, 1317-1326.
52. Villa,P., Kaufmann,S.H. and Earnshaw,W.C. (1997) Caspases and caspase inhibitors. Trends Biochem. Sci., 22, 388-393.
53. Wildbaum,G., Youssef,S., Grabie,N. and Karin,N. (1998) Neutralizing antibodies to IFN-γ-inducing factor prevent experimental autoimmune encephalomyelitis. J. Immunol., 161, 6368-6374.
54. Zhou,Q., Krebs,J.F., Snipas,S.J., Price,A., Alnemri,E.S., Tomaselli,K.J. and Salvesen,G.S. (1998) Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics and characterization of the caspase/p35 complex. Biochemistry, 37, 10757-10765.