Beyond apoptosis: Nonapoptotic cell death in physiology and disease

Biochemistry and Cell Biology

Volumn 83, Issue 5, 2005, Pages 579-588

  Hetz, Claudio A ^a,c   Torres, Vicente ^b   Quest, Andrew F G ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Ceramides; Death receptors; Necrosis; Nonapoptotic programmed cell death

Indexed keywords

DATA ACQUISITION; DISEASES;

CELL-DEATH PATHWAYS; DEATH-RECEPTOR; PROGRAMMED CELL DEATH (PCD);

CELL CULTURE;

ARSENIC TRIOXIDE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALRETICULIN; CASPASE; CERAMIDE; DEATH RECEPTOR; DNA FRAGMENT; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; TAMOXIFEN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOLYSIS; AUTOPHAGY; CANCER THERAPY; CELL DEATH; CELL FUNCTION; CELL NUCLEUS; CELL SWELLING; CELL VACUOLE; CHROMATIN CONDENSATION; CYTOPLASM; DNA DAMAGE; ENZYME ACTIVATION; GENE MUTATION; HOMEOSTASIS; HUMAN; INFLAMMATION; LYMPHOCYTE; LYSOSOME; MEMBRANE DAMAGE; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN FAMILY; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; AUTOPHAGY; CASPASES; CERAMIDES; ENZYME ACTIVATION; HUMANS; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION;

EID: 29144494879     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-065     Document Type: Review

References (88)

1. Amarante-Mendes, G.P., Finucane, D.M., Martin, S.J., Cotter, T.G., Salvesen, G.S., and Green, D.R. 1998. Anti-apoptotic oncogenes prevent caspase-dependent and independent commitment for cell death. Cell Death Differ. 5: 298-306.
2. Ankarcrona, M. 1998. Glutamate induced cell death: apoptosis or necrosis? Prog. Brain Res. 116: 265-272.
3. Bahr, B.A., and Bendiske, J. 2002. The neuropathogenic contributions of lysosomal dysfunction. J. Neurochem. 83: 481-489.
4. Barros, L.F., Hermosilla, T., and Castro, J. 2001a. Necrotic volume increase and the early physiology of necrosis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130: 401-409.
5. Barros, L.F., Stutzin, A., Calixto, A., Catalan, M., Castro, J., Hetz, C., and Hermosilla, T. 2001b. Nonselective cation channels as effectors of free radical-induced rat liver cell necrosis. Hepatology, 33: 114-122.
6. Belaud-Rotureau, M.A., Lacombe, F., Durrieu, F., Vial, J.P., Lacoste, L., Bernard, P., and Belloc, F. 1999. Ceramide-induced apoptosis occurs independently of caspases and is decreased by leupeptin. Cell Death Differ. 6: 788-795.
7. Boya, P., Andreau, K., Poncet, D., Zamzami, N., Perfettini, J.L., Metivier, D. et al. 2003a. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 197: 1323-1334.
8. Boya, P., Gonzalez-Polo, R.A., Poncet, D., Andreau, K., Vieira, H.L., Roumier, T. et al. 2003b. Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene, 22: 3927-3936.
9. Breckenridge, D.G., Germain, M., Mathai, J.P., Nguyen, M., and Shore, G.C. 2003. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene, 22: 8608-8618.
10. Brenner, B., Koppenhoefer, U., Weinstock, C., Linderkamp, O., Lang, F., and Gulbins, E. 1997. Fas- or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J. Biol. Chem. 272: 22173-22181.
11. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8: 569-581.
12. Cande, C., Cecconi, F., Dessen, P., and Kroemer, G. 2002. Apoptosis-inducing factor (AIF): Key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115: 4727-4734.
13. Castilla, J., Hetz, C., and Soto, C. 2004. Molecular mechanisms of neurotoxicity of pathological prion protein. Curr. Mol. Med. 4: 397-403.
14. Cock, J.G., Tepper, A.D., de Vries, E., van Blitterswijk, W.J., and Borst, J. 1998. CD95 (Fas/APO-1) induces ceramide formation and apoptosis in the absence of a functional acid sphingomyelinase. J. Biol. Chem. 273: 7560-7565.
15. Daido, S., Kanzawa, T., Yamamoto, A., Takeuchi, H., Kondo, Y., and Kondo, S. 2004. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64: 4286-4293.
16. Danial, N.N., and Korsmeyer, S.J. 2004. Cell death: critical control points. Cell, 116: 205-219.
17. Degterev, A., Boyce, M., and Yuan, J. 2003. A decade of caspases. Oncogene, 22: 8543-8567.
18. Denecker, G., Vercammen, D., Steemans, M., Vanden Berghe, T., Brouckaert, G., Van Loo, G. et al. 2001. Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ. 8: 829-840.
19. Dypbukt, J.M., Ankarcrona, M., Burkitt, M., Sjoholm, A., Strom, K., Orrenius, S., and Nicotera, P. 1994. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J. Biol. Chem. 269: 30553-30560.
20. Edinger, A.L., and Thompson, C.B. 2003. Defective autophagy leads to cancer. Cancer Cell, 4: 422-424.
21. Fadok, V.A., Bratton, D.L., Rose, D.M., Pearson, A., Ezekewitz, R.A., and Henson, P.M. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature (London), 405: 85-90.
22. Garcia-Ruiz, C., Colell, A., Mari, M., Morales, A., and Fernandez-Checa, J.C. 1997. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 272: 11369-11377.
23. Gozuacik, D., and Kimchi, A. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene, 23: 2891-2906.
24. Grullich, C., Sullards, M.C., Fuks, Z., Merrill, A.H., Jr., and Kolesnick, R. 2000. CD95(Fas/APO-1) signals ceramide generation independent of the effector stage of apoptosis. J. Biol. Chem. 275: 8650-8656.
25. Gudz, T.I., Tserng, K.Y., and Koppel, C.L. 1997. Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J. Biol. Chem. 272: 24154-24158.
26. Hannun, Y.A., and Obeid, L.M. 2002. The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277: 25847-25850.
27. Haraguchi, M., Torii, S., Matsuzawa, S., Xie, Z., Kitada, S., Krajewski, S. et al. 2000. Apoptotic protease activating factor 1 (Apaf-1)-independent cell death suppression by Bcl-2. J. Exp. Med. 191: 1709-1720.
28. Hengartner, M.O. 2000. The biochemistry of apoptosis. Nature (London), 407: 770-776.
29. Hetz, C., Bono, M.R., Barros, L.F., and Lagos, R. 2002a. Microcin E492, a channel-forming bacteriocin from Klebsiella pneumoniae, induces apoptosis in some human cell lines. Proc. Natl. Acad. Sci. U.S.A. 99: 2696-2701.
30. Hetz, C.A., Hunn, M., Rojas, P., Torres, V., Leyton, L., and Quest, A.F. 2002b. Caspase-dependent initiation of apoptosis and necrosis by the Fas receptor in lymphoid cells: onset of necrosis is associated with delayed ceramide increase. J. Cell Sci. 115: 4671-4683.
31. Hetz, C., Russelakis-Carneiro, M., Maundrell, K., Castilla, J., and Soto, C. 2003. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 22: 5435-5445.
32. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S. et al. 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1: 489-495.
33. Jaattela, M., and Tschopp, J. 2003. Caspase-independent cell death in T lymphocytes. Nat. Immunol. 4: 416-423.
34. Jonas, D., Walev, I., Berger, T., Liebetrau, M., Palmer, M., and Bhakdi, S. 1994. Novel path to apoptosis: small transmembrane pores created by staphylococcal alpha-toxin in T lymphocytes evoke internucleosomal DNA degradation. Infect. Immun. 62: 1304-1312.
35. Kanzawa, T., Kondo, Y., Ito, H., Kondo, S., and Germano, I. 2003. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res. 63: 2103-2108.
36. Kawahara, A., Ohsawa, Y., Matsumura, H., Uchiyama, Y., and Nagata, S. 1998. Caspase-independent cell killing by Fas-associated protein with death domain. J. Cell Biol. 143: 1353-1360.
37. Kegel, K.B., Kim, M., Sapp, E., McIntyre, C., Castano, J.G., Aronin, N., and DiFiglia, M. 2000. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J. Neurosci. 20: 7268-7278.
38. Kerr, J.F., Wyllie, A.H., and Currie, A.R. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26: 239-257.
39. Klionsky, D.J., and Emr, S.D. 2000. Autophagy as a regulated pathway of cellular degradation. Science (Wash. D.C.), 290: 1717-1721.
40. Krysko, O., De Ridder, L., and Cornelissen, M. 2004. Phosphatidylserine exposure during early primary necrosis (oncosis) in JB6 cells as evidenced by immunogold labeling technique. Apoptosis, 9: 495-500.
41. Laster, S.M., Wood, J.G., and Gooding, L.R. 1988. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 141: 2629-2634.
42. Leist, M., Single, B., Castoldi, A.F., Kuhnle, S., and Nicotera, P. 1997. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185: 1481-1486.
43. Lewis, J., Devin, A., Miller, A., Lin, Y., Rodriguez, Y., Neckers, L., and Liu, Z.G. 2000. Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J. Biol. Chem. 275: 10519-10526.
44. Leyton, L., and Quest, A.F. 2002. Introduction to supramolecular complex formation in cell signaling and disease. Biol. Res. 35: 117-125.
45. Leyton, L., and Quest, A.F. 2004. Supramolecular complex formation in cell signaling and disease: an update on a recurrent theme in cell life and death. Biol. Res. 37: 29-43.
46. 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.
47. Li, L., Thomas, R.M., Suzuki, H., De Brabander, J.K., Wang, X., and Harran, P.G. 2004. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science (Wash. D.C.), 305: 1471-1474.
48. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature (London), 402: 672-676.
49. Lin, Y., Choksi, S., Shen, H.M., Yang, Q.F., Hur, G.M., Kim, Y.S. et al. 2004. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J. Biol. Chem. 279: 10822-10828.
50. Lockshin, R.A., and Williams, C.M. 1965. Programmed cell death. V. Cytolytic enzymes in relation to the breakdown of the intersegmental muscles of silkmoths. J. Insect Physiol. 11: 831-844.
51. Majno, G., and Joris, I. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146: 3-15.
52. Matsumura, H., Shimizu, Y., Ohsawa, Y., Kawahara, A., Uchiyama, Y., and Nagata, S. 2000. Necrotic death pathway in Fas receptor signaling. J. Cell Biol. 151: 1247-1256.
53. McDonald, P.P., Fadok, V.A., Bratton, D., and Henson, P.M. 1999. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J. Immunol. 163: 6164-6172.
54. Mengubas, K., Riordan, F.A., Bravery, C.A., Lewin, J., Owens, D.L., Mehta, A.B. et al. 1999. Ceramide-induced killing of normal and malignant human lymphocytes is by a non-apoptotic mechanism. Oncogene, 18: 2499-2506.
55. Mochizuki, T., Asai, A., Saito, N., Tanaka, S., Katagiri, H., Asano, T. et al. 2002. Akt protein kinase inhibits non-apoptotic programmed cell death induced by ceramide. J. Biol. Chem. 277: 2790-2797.
56. Nagata, S., and Golstein, P. 1995. The Fas death factor. Science (Wash. D.C.), 267: 1449-1456.
57. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B.A., and Yuan, J. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature (London), 403: 98-103.
58. Nishitoh, H., Matsuzawa, A., Tobiume, K., Saegusa, K., Takeda, K., Inoue, K. et al. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16: 1345-1355.
59. Ogretmen, B., and Hannun, Y.A. 2004. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer, 4: 604-616.
60. Paglin, S., Hollister, T., Delohery, T., Hackett, N., McMahill, M., Sphicas, E. et al. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61: 439-444.
61. Peter, M.E., and Krammer, RH. 2003. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ. 10: 26-35.
62. Petersen, A., Larsen, K.E., Behr, G.G., Romero, N., Przedborski, S., Brundin, P., and Sulzer, D. 2001. Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration. Hum. Mol. Genet. 10: 1243-1254.
63. Pinton, P., Ferrari, D., Rapizzi, E., Di Virgilio, F., Pozzan, T., and Rizzuto, R. 2001. The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 20: 2690-2701.
64. Quillet-Mary, A., Jaffrezou, J.P., Mansat, V., Bordier, C., Naval, J., and Laurent, G. 1997. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J. Biol. Chem. 272: 21388-21395.
65. Ramos, B., Lahti, J.M., Claro, E., and Jackowski, S. 2003. Prevalence of necrosis in C2-ceramide-induced cytotoxicity in NB16 neuroblastoma cells. Mol. Pharmacol. 64: 502-511.
66. Rao, R.V., and Bredesen, D.E. 2004. Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr. Opin. Cell Biol. 16: 653-662.
67. Razik, M.A., and Cidlowski, J.A. 2002. Molecular interplay between ion channels and the regulation of apoptosis. Biol. Res. 35: 203-207.
68. Sauter, B., Albert, M.L., Francisco, L., Larsson, M., Somersan, S., and Bhardwaj, N. 2000. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191: 423-434.
69. Scarlatti, F., Bauvy, C., Ventruti, A., Sala, G., Cluzeaud, F., Vandewalle, A. et al. 2004. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1. J. Biol. Chem. 279: 18384-18391.
70. Shimizu, S., Kanaseki, T., Mizushima, N., Mizuta, T., Arakawa-Kobayashi, S., Thompson, C.B., and Tsujimoto, Y. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6: 1221-1228.
71. Shintani, T., and Klionsky, D.J. 2004. Autophagy in health and disease: a double-edged sword. Science (Wash. D.C.), 306: 990-995.
72. Simon, F., Varela, D., Eguiguren, A.L., Diaz, L.F., Sala, F., and Stutzin, A. 2004. Hydroxyl radical activation of a Ca(2+)-sensitive nonselective cation channel involved in epithelial cell necrosis. Am. J. Physiol. Cell Physiol. 287: C963-C970.
73. Stefani, M., and Dobson, C.M. 2003. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81: 678-699.
74. Stefanis, L., Larsen, K.E., Rideout, H.J., Sulzer, D., and Greene, L.A. 2001. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21: 9549-9560.
75. Suda, T., Takahashi, T., Golstein, P., and Nagata, S. 1993. Molecular cloning and expression of the Pas ligand, a novel member of the tumor necrosis factor family. Cell, 75: 1169-1178.
76. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M. et al. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature (London), 397: 441-446.
77. Tepper, A.D., Ruurs, P., Wiedmer, T., Sims, P.J., Borst, J., and van Blitterswijk, W.J. 2000. Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology. J. Cell Biol. 150: 155-164.
78. Tepper, A.D., Ruurs, P., Borst, J., and van Blitterswijk, W.J. 2001. Effect of overexpression of a neutral sphingomyelinase on CD95-induced ceramide production and apoptosis. Biochem. Biophys. Res. Commun. 280: 634-639.
79. Vande Velde, C., Cizeau, J., Dubik, D., Alimonti, J., Brown, T., Israels, S. et al. 2000. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell. Biol. 20: 5454-5468.
80. Vanden Berghe, T., Kalai, M., van Loo, G., Declercq, W., and Vandenabeele, P. 2003. Disruption of HSP90 function reverts tumor necrosis factor-induced necrosis to apoptosis. J. Biol. Chem. 278: 5622-5629.
81. Vanden Berghe, T., van Loo, G., Saelens, X., Van Gurp, M., Brouckaert, G., Kalai, M. et al. 2004. Differential signaling to apoptotic and necrotic cell death by Fas-associated death domain protein FADD. J. Biol. Chem. 279: 7925-7933.
82. Vaux, D.L., and Korsmeyer, S.J. 1999. Cell death in development. Cell, 96: 245-254.
83. Vercammen, D., Beyaert, R., Denecker, G., Goossens, V., Van Loo, G., Declercq, W. et al. 1998a. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187: 1477-1485.
84. Vercammen, D., Brouckaert, G., Denecker, G., Van de Craen, M., Declercq, W., Fiers, W., and Vandenabeele, P. 1998b. Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J. Exp. Med. 188: 919-930.
85. Walensky, L.D., Kung, A.L., Escher, I., Malia, T.J., Barbuto, S., Wright, R.D. et al. 2004. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science (Wash. D.C.), 305: 1466-1470.
86. Xu, K., Tavernarakis, N., and Driscoll, M. 2001. Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca(2+) release from the endoplasmic reticulum. Neuron, 31: 957-971.
87. Yuan, J., Lipinski, M., and Degterev, A. 2003. Diversity in the mechanisms of neuronal cell death. Neuron, 40: 401-413.
88. Yue, Z., Jin, S., Yang, C., Levine, A.J., and Heintz, N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 100: 15077-15082.