Molecular mechanisms of Fas-mediated cell death in oligodendrocytes

Journal of Neurotrauma

Volumn 25, Issue 5, 2008, Pages 411-426

  Austin, James W ^a,c   Fehlings, Michael G ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b TORONTO WESTERN HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Apoptosis; Caspase; Cytochrome c; Fas; Oligodendrocytes

Indexed keywords

CASPASE; CYTOCHROME C; FAS LIGAND;

APOPTOSIS; ARTICLE; CELL DEATH; CELL LYSATE; CONTROLLED STUDY; DNA FRAGMENTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NEUROLOGIC DISEASE; NICK END LABELING; OLIGODENDROGLIA; PROTEIN EXPRESSION; SPINAL CORD INJURY;

ANTIGENS, CD95; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BLOTTING, WESTERN; CASPASES; CELL LINE, TUMOR; CYTOCHROMES C; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME INHIBITORS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, CONFOCAL; OLIGODENDROGLIA; SIGNAL TRANSDUCTION;

EID: 43649105315     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2007.0436     Document Type: Article

References (64)

1. Abe, Y., Yamamoto, T., Sugiyama, Y., Watanabe, T., Saito, N., Kayama, H., and Kumagai, T. (1999). Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J. Neurotrauma 16, 945-952.
2. Arscott, P.L., Knapp, J., Rymaszewski, M., Bartron, J.L., Bretz, J.D., Thompson, N.W., and Baker, J.R., Jr. (1997). Fas (APO-1, CD95)-mediated apoptosis in thyroid cells is regulated by a labile protein inhibitor. Endocrinology 138, 5019-5027.
3. Blight, A.R. (2002). Miracles and molecules-progress in spinal cord repair. Nat. Neurosci. 5, Suppl, 1051-1054.
4. Brooks, A.D., and Sayers, T.J. (2005). Reduction of the anti-apoptotic protein cFLIP enhances the susceptibility of human renal cancer cells to TRAIL apoptosis. Cancer Immunol. Immunother. 54, 499-505.
5. Buntinx, M., Vanderlocht, J., Hellings, N., Vandenabeele, F., Lambrichts, I., Raus, J., Ameloot, M., Stinissen, P., and Steels, P. (2003). Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocyte-specific gene expression. J. Neurocytol. 32, 25-38.
6. Buntinx, M., Gielen, E., Van Hummelen, P., Raus, J., Ameloot, M., Steels, P., and Stinissen, P. (2004). Cytokine-induced cell death in human oligodendroglial cell lines. II: Alterations in gene expression induced by interferon-gamma and tumor necrosis factor-alpha. J. Neurosci. Res. 76, 846-861.
7. Carlo-Stella, C., Di Nicola, M., Turco, M. C., Cleris, L., Lavazza, C., Longoni, P., Milanesi, M., Magni, M., Ammirante, M., Leone, A., Nagy, Z., Gioffre, W.R., Formelli, F., and Gianni, A.M. (2006). The anti-human leukocyte antigen-DR monoclonal antibody 1D09C3 activates the mitochondrial cell death pathway and exerts a potent antitumor activity in lymphoma-bearing nonobese diabetic/severe combined immunodeficient mice. Cancer Res. 66, 1799-1808.
8. Casha, S., Yu, W.R., and Fehlings, M.G. (2001). Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 103, 203-218.
9. Casha, S., Yu, W.R., and Fehlings, M.G. (2005). FAS deficiency reduces apoptosis, spares axons and improves function after spinal cord injury. Exp. Neurol. 196, 390-400.
10. Citron, B.A., Arnold, P.M., Sebastian, C., Qin, F., Malladi, S., Ameenuddin, S., Landis, M.E., and Festoff, B.W. (2000). Rapid upregulation of caspase-3 in rat spinal cord after injury: mRNA, protein, and cellular localization correlates with apoptotic cell death. Exp. Neurol. 166, 213-226.
11. Cregan, S.P., Dawson, V.L., and Slack, R.S. (2004). Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23, 2785-2796.
12. 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.
13. Davis, A.R., Lotocki, G., Marcillo, A.E., Dietrich, W.D., and Keane, R.W. (2007). FasL, Fas, and death-inducing signaling complex (DISC) proteins are recruited to membrane rafts after spinal cord injury. J. Neurotrauma 24, 823-834.
14. Demjen, D., Klussmann, S., Kleber, S., Zuliani, C., Stieltjes, B., Metzger, C., Hirt, U.A., Walczak, H., Falk, W., Essig, M., Edler, L., Krammer, P.H., and Martin-Villalba, A. (2004). Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat. Med. 10, 389-395.
15. Desagher, S., Osen-Sand, A., Nichols, A., Eskes, R., Montessuit, S., Lauper, S., Maundrell, K., Antonsson, B., and Martinou, J.C. (1999). Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144, 891-901.
16. Desbarats, J., Birge, R.B., Mimouni-Rongy, M., Weinstein, D.E., Palerme, J.S., and Newell, M.K. (2003). Fas engagement induces neurite growth through ERK activation and p35 upregulation. Nat. Cell Biol. 5, 118-125.
17. Donepudi, M., Mac Sweeney, A., Briand, C., and Grutter, M.G. (2003). Insights into the regulatory mechanism for caspase-8 activation. Mol. Cell. 11, 543-549.
18. Emery, E., Aldana, P., Bunge, M.B., Puckett, W., Srinivasan, A., Keane, R.W., Bethea, J., and Levi, A.D. (1998). Apoptosis after traumatic human spinal cord injury. J. Neurosurg. 89, 911-920.
19. Fulda, S., Meyer, E., and Debatin, K.M. (2000). Metabolic inhibitors sensitize for CD95 (APO-1/Fas)-induced apoptosis by down-regulating Fas-associated death domain-like interleukin 1-converting enzyme inhibitory protein expression. Cancer Res. 60, 3947-3956.
20. Gomez-Angelats, M., and Cidlowski, J.A. (2001). Protein kinase C regulates FADD recruitment and death-inducing signaling complex formation in Fas/CD95-induced apoptosis. J. Biol. Chem. 276, 44944-44952.
21. Green, D.R., and Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 626-629.
22. Henshall, D.C., Bonislawski, D.P., Skradski, S.L., Lan, J.Q., Meller, R., and Simon, R.P. (2001). Cleavage of bid may amplify caspase-8-induced neuronal death following focally evoked limbic seizures. Neurobiol. Dis. 8, 568-580.
23. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J.L., Schneider, P., Seed, B., and Tschopp, J. (2000). Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495.
24. Kayalar, C., Ord, T., Testa, M.P., Zhong, L.T., and Bredesen, D.E. (1996). Cleavage of actin by interleukin 1 beta-converting enzyme to reverse DNase I inhibition. Proc. Natl. Acad. Sci. USA 93, 2234-2238.
25. Keane, R.W., Kraydieh, S., Lotocki, G., Alonso, O.F., Aldana, P., and Dietrich, W.D. (2001). Apoptotic and antiapoptotic mechanisms after traumatic brain injury. J. Cereb. Blood Flow Metab. 21, 1189-1198.
26. Krohn, A.J., Wahlbrink, T., and Prehn, J.H. (1999). Mitochondrial depolarization is not required for neuronal apoptosis. J. Neurosci. 19, 7394-7404.
27. Li, G.L., Brodin, G., Farooque, M., Funa, K., Holtz, A., Wang, W.L., and Olsson, Y. (1996). Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord. J. Neuropathol. Exp. Neurol. 55, 280-289.
28. Li, G.L., Farooque, M., and Olsson, Y. (2000a). Changes of Fas and Fas ligand immunoreactivity after compression trauma to rat spinal cord. Acta Neuropathol. (Berl.) 100, 75-81.
29. Li, M., Ona, V.O., Chen, M., Kaul, M., Tenneti, L., Zhang, X., Stieg, P.E., Lipton, S.A., and Friedlander, R.M. (2000b). Functional role and therapeutic implications of neuronal caspase-1 and -3 in a mouse model of traumatic spinal cord injury. Neuroscience 99, 333-342.
30. Li, L.Y., Luo, X., and Wang, X. (2001). Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412, 95-99.
31. Li, W., Maeda, Y., Ming, X., Cook, S., Chapin, J., Husar, W., and Dowling, P. (2002). Apoptotic death following Fas activation in human oligodendrocyte hybrid cultures. J. Neurosci. Res. 69, 189-196.
32. Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997a). DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175-184.
33. Liu, X.Z., Xu, X.M., Hu, R., Du, C., Zhang, S.X., Mcdonald, J.W., Dong, H.X., Wu, Y.J., Fan, G.S., Jacquin, M.F., Hsu, C.Y., and Choi, D.W. (1997b). Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17, 5395-5406.
34. Ly, J.D., Grubb, D.R., and Lawen, A. (2003). The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 8, 115-128.
35. Matsushita, K., Wu, Y., Qiu, J., Lang-Lazdunski, L., Hirt, L., Waeber, C., Hyman, B.T., Yuan, J., and Moskowitz, M.A. (2000). Fas receptor and neuronal cell death after spinal cord ischemia. J. Neurosci. 20, 6879-6887.
36. Mcewen, M.L., and Springer, J.E. (2005). A mapping study of caspase-3 activation following acute spinal cord contusion in rats. J. Histochem. Cytochem. 53, 809-819.
37. Mclaurin, J., Trudel, G.C., Shaw, I.T., Antel, J.P., and Cashman, N.R. (1995). A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J. Neurobiol. 26, 283-293.
38. Ozawa, H., Keane, R.W., Marcillo, A.E., Diaz, P.H., and Dietrich, W.D. (2002). Therapeutic strategies targeting caspase inhibition following spinal cord injury in rats. Exp. Neurol. 177, 306-313.
39. Pouly, S., Becher, B., Blain, M., and Antel, J.P. (2000). Interferon-gamma modulates human oligodendrocyte susceptibility to Fas-mediated apoptosis. J. Neuropathol. Exp. Neurol. 59, 280-286.
40. Qiu, J., Whalen, M.J., Lowenstein, P., Fiskum, G., Fahy, B., Darwish, R., Aarabi, B., Yuan, J., and Moskowitz, M.A. (2002). Upregulation of the Fas receptor death-inducing signaling complex after traumatic brain injury in mice and humans. J. Neurosci. 22, 3504-3511.
41. Rodriguez-Hernandez, A., Brea-Calvo, G., Fernandez-Ayala, D.J., Cordero, M., Navas, P., and Sanchez-Alcazar, J.A. (2006). Nuclear caspase-3 and capase-7 activation, and Poly(ADP-ribose) polymerase cleavage are early events in camptothecin-induced apoptosis. Apoptosis 11, 131-139.
42. Roy, S., and Nicholson, D.W. (2000). Cross-talk in cell death signaling. J. Exp. Med. 192, F21-F25.
43. 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.
44. Segura, M.F., Sole, C., Pascual, M., Moubarak, R.S., Perez-Garcia, M.J., Gozzelino, R., Iglesias, V., Badiola, N., Bayascas, J.R., Llecha, N., Rodriguez-Alvarez, J., Soriano, E., Yuste, V.J., and Comella, J.X. (2007). The long form of Fas apoptotic inhibitory molecule is expressed specifically in neurons and protects them against death receptor-triggered apoptosis. J. Neurosci. 27, 11228-11241.
45. Sekhon, L.H., and Fehlings, M.G. (2001). Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 26, S2-S12.
46. Springer, J.E., Azbill, R.D., and Knapp, P.E. (1999). Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 5, 943-946.
47. Srinivasula, S.M., Hegde, R., Saleh, A., Datta, P., Shiozaki, E., Chai, J., Lee, R.A., Robbins, P.D., Fernandes-Alnemri, T., Shi, Y., and Alnemri, E.S. (2001). A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410, 112-116.
48. Sullivan, P.G., Rabchevsky, A.G., Waldmeier, P.C., and Springer, J.E. (2005). Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J. Neurosci. Res. 79, 231-239.
49. Tafani, M., Karpinich, N.O., Serroni, A., Russo, M.A., and Farber, J.L. (2006). Re-evaluation of the distinction between type I and type II cells: the necessary role of the mitochondria in both the extrinsic and intrinsic signaling pathways upon Fas receptor activation. J. Cell. Physiol. 208, 556-565.
50. Teng, Y.D., Choi, H., Onario, R.C., Zhu, S., Desilets, F.C., Lan, S., Woodard, E.J., Snyder, E.Y., Eichler, M.E., and Friedlander, R.M. (2004). Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc. Natl. Acad. Sci. USA 101, 3071-3076.
51. Tschopp, J., Irmler, M., and Thome, M. (1998). Inhibition of fas death signals by FLIPs. Curr. Opin. Immunol. 10, 552-558.
52. Vercammen, D., Brouckaert, G., Denecker, G., Van De Craen, M., Declercq, W., Fiers, W., and Vandenabeele, P. (1998). Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J. Exp. Med. 188, 919-930.
53. Wada, S., Yone, K., Ishidou, Y., Nagamine, T., Nakahara, S., Niiyama, T., and Sakou, T. (1999). Apoptosis following spinal cord injury in rats and preventative effect of N-methyl-D-aspartate receptor antagonist. J. Neurosurg. 91, 98-104.
54. Warden, P., Bamber, N.I., Li, H., Esposito, A., Ahmad, K.A., Hsu, C.Y., and Xu, X.M. (2001). Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp. Neurol. 168, 213-224.
55. Waterhouse, N.J., Steel, R., Kluck, R., and Trapani, J.A. (2004). Assaying cytochrome C translocation during apoptosis. Methods Mol. Biol. 284, 307-313.
56. Wei, M.C., Lindsten, T., Mootha, V.K., Weiler, S., Gross, A., Ashiya, M., Thompson, C.B., and Korsmeyer, S.J. (2000). tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14, 2060-2071.
57. Widlak, P., Li, L.Y., Wang, X., and Garrard, W.T. (2001). Action of recombinant human apoptotic endonuclease G on naked DNA and chromatin substrates: cooperation with exonuclease and DNase I. J. Biol. Chem. 276, 48404-48409.
58. Woo, M., Hakem, A., Elia, A.J., Hakem, R., Duncan, G.S., Patterson, B.J., and Mak, T.W. (1999). In vivo evidence that caspase-3 is required for Fas-mediated apoptosis of hepatocytes. J. Immunol. 163, 4909-4916.
59. Ye, H., Cande, C., Stephanou, N.C., Jiang, S., Gurbuxani, S., Larochette, N., Daugas, E., Garrido, C., Kroemer, G., and Wu, H. (2002). DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nat. Struct. Biol. 9, 680-684.
60. Yin, X.M. (2000). Bid, a critical mediator for apoptosis induced by the activation of Fas/TNF-R1 death receptors in hepatocytes. J. Mol. Med. 78, 203-211.
61. Yin, X.M., Wang, K., Gross, A., Zhao, Y., Zinkel, S., Klocke, B., Roth, K.A., and Korsmeyer, S.J. (1999). Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400, 886-891.
62. Yoshino, O., Matsuno, H., Nakamura, H., Yudoh, K., Abe, Y., Sawai, T., Uzuki, M., Yonehara, S., and Kimura, T. (2004). The role of Fas-mediated apoptosis after traumatic spinal cord injury. Spine 29, 1394-1404.
63. Yu, F., Sugawara, T., Nishi, T., Liu, J., and Chan, P.H. (2006). Overexpression of SOD1 in transgenic rats attenuates nuclear translocation of endonuclease G and apoptosis after spinal cord injury. J. Neurotrauma 23, 595-603.
64. Zurita, M., Vaquero, J., and Zurita, I. (2001). Presence and significance of CD-95 (Fas/APO1) expression after spinal cord injury. J. Neurosurg. 94, 257-264.