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Cellular and Molecular Biology Letters

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Volume 11, Issue 4 (Dec 2006)

Current concepts in apoptosis: The physiological suicide program revisited

Indrajit Chowdhury / Binu Tharakan
  • Department of Neurology, Scott and White Clinic, The Texas A & M University Health Science Center, College of Medicine, Temple, Texas, USA
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/ Ganapathy Bhat
Published Online: 2006-09-05 | DOI: https://doi.org/10.2478/s11658-006-0041-3

Abstract

Apoptosis, or programmed cell death (PCD), involves a complex network of biochemical pathways that normally ensure a homeostatic balance between cellular proliferation and turnover in nearly all tissues. Apoptosis is essential for the body, as its deregulation can lead to several diseases. It plays a major role in a variety of physiological events, including embryonic development, tissue renewal, hormone-induced tissue atrophy, removal of inflammatory cells, and the evolution of granulation tissue into scar tissue. It also has an essential role in wound repair. The various cellular and biochemical mechanisms involved in apoptosis are not fully understood. However, there are two major pathways, the extrinsic pathway (receptor-mediated apoptotic pathway) and the intrinsic pathway (mitochondria-mediated apoptotic pathway), which are both well established. The key component in both is the activation of the caspase cascade. Caspases belong to the family of proteases that ultimately, by cleaving a set of proteins, cause disassembly of the cell. Although the caspase-mediated proteolytic cascade represents a central point in the apoptotic response, its initiation is tightly regulated by a variety of other factors. Among them, Bcl-2 family proteins, TNF and p53 play pivotal roles in the regulation of caspase activation and in the regulation of apoptosis. This review summarizes the established concepts in apoptosis as a physiological cell suicide program, highlighting the recent and significant advances in its study.

Keywords: Apoptosis; Programmed cell death; Pathways; Caspases; Bcl-2; p53; TNF; Apaf

  • [1] Vaux, D.L. and Korsmeyer, S.J. Cell death in development. Cell 96 (1999) 245–254. http://dx.doi.org/10.1016/S0092-8674(00)80564-4CrossrefGoogle Scholar

  • [2] Kerr, J.F.R. An electron-microscope study of liver cell necrosis due to Albitocin. Pathology 2 (1970) 251–259. CrossrefGoogle Scholar

  • [3] Kerr, J.F.R. Shrinkage necrosis: A distinct mode of cellular death. J. Path. 105 (1971) 13–20. http://dx.doi.org/10.1002/path.1711050103CrossrefGoogle Scholar

  • [4] Kerr, J.F. Wyllie, A.H. and Currie, A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239–257. CrossrefGoogle Scholar

  • [5] Thompson, C.B. Apoptosis in the pathogenesis and treatment of disease. Science 267 (1995) 1456–1462. http://dx.doi.org/10.1126/science.7878464CrossrefGoogle Scholar

  • [6] Wang, X. The expanding role of mitochondria in apoptosis. Genes Dev. 15 (2001) 2922–2933. Google Scholar

  • [7] Hortvitz, H.R. Worm, life and death (Nobel lecture). Chembiochem. 4 (2003) 697–711. http://dx.doi.org/10.1002/cbic.200300614CrossrefGoogle Scholar

  • [8] Danial, N.N. and Krosmeyer, S.J. Cell death: critical control points. Cell 116 (2004) 205–219. http://dx.doi.org/10.1016/S0092-8674(04)00046-7CrossrefGoogle Scholar

  • [9] Schwartzman, R.A. and Cidlowski, J.A. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14 (1993) 133–51. http://dx.doi.org/10.1210/er.14.2.133CrossrefGoogle Scholar

  • [10] Cohen, J.J. Apoptosis. Immunol. Today 14 (1993) 126–130. http://dx.doi.org/10.1016/0167-5699(93)90214-6CrossrefGoogle Scholar

  • [11] Vaux, D.L. and Strasser, A. The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA 93 (1996) 2239–2244. http://dx.doi.org/10.1073/pnas.93.6.2239CrossrefGoogle Scholar

  • [12] Levine, B. and Yuan, J. Autophagy in cell death: an innocent convict? J. Clin. Invest. 115 (2005) 2679–2688. http://dx.doi.org/10.1172/JCI26390CrossrefGoogle Scholar

  • [13] Clarke, P.G. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181 (1990) 195–213. http://dx.doi.org/10.1007/BF00174615CrossrefGoogle Scholar

  • [14] Bursch, W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8 (2001) 569–581. http://dx.doi.org/10.1038/sj.cdd.4400852CrossrefGoogle Scholar

  • [15] Majno, G. and Joris, I. Apoptosis, oncosis and necrosis. An overview of cell death. Am. J. Pathol. 146 (1995) 3–15. Google Scholar

  • [16] Broker, L.E., Kruyt, F. and Giaccone, G. Cell death independent of caspases: a review. Clin. Cancer Res. 11 (2005) 3155–3162. http://dx.doi.org/10.1158/1078-0432.CCR-04-2223CrossrefGoogle Scholar

  • [17] Castedo, M., Perfettini, J.L., Roumier, T., Andreau, K., Medema, R. and Kroemer, G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 23 (2004) 2825–2837. http://dx.doi.org/10.1038/sj.onc.1207528CrossrefGoogle Scholar

  • [18] Earnshaw, W.C. Nuclear changes in apoptosis. Cur. Opin. Cell Biol. 7 (1995) 337–343. http://dx.doi.org/10.1016/0955-0674(95)80088-3CrossrefGoogle Scholar

  • [19] Au, J.L., Panchal, N., Li, D. and Gan, Y. Apoptosis: a new pharmacodynamic endpoint. Pharm. Res. 14 (1997) 1659–1671. http://dx.doi.org/10.1023/A:1012159208559CrossrefGoogle Scholar

  • [20] Gong, J., Traganos, F. and Darsynkiewicz, Z. A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal. Biochem. 218 (1994) 314–319. http://dx.doi.org/10.1006/abio.1994.1184CrossrefGoogle Scholar

  • [21] Bortner, C.D., Oldenburg, N.D. and Cidlowski, J.A. The role of DNA fragmentation in apoptosis. Trends Cell Biol. 5 (1995) 21–26. http://dx.doi.org/10.1016/S0962-8924(00)88932-1CrossrefGoogle Scholar

  • [22] Dive, C., Gregory, C.D., Phopps, D.J., Evans, D.L., Milner, A.E. and Wyllie, A.H. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochem. Biophys. Acta 1133 (1992) 275–285. http://dx.doi.org/10.1016/0167-4889(92)90048-GCrossrefGoogle Scholar

  • [23] Hamel, W., Dazin, P. and Israel, M. Adaptation of a simple flow cytometric assay to identify different stages during apoptosis. Cytometry 25 (1996) 173–181. http://dx.doi.org/10.1002/(SICI)1097-0320(19961001)25:2<173::AID-CYTO6>3.0.CO;2-ICrossrefGoogle Scholar

  • [24] Gavrieli, Y., Sherman, Y. and Benassan, S.A. Identification of programmed cell death in situ via special labeling of nuclear DNA fragments. J. Cell Biol. 119 (1992) 493–501. http://dx.doi.org/10.1083/jcb.119.3.493CrossrefGoogle Scholar

  • [25] Charriaut-Malangue, C. and Ben-Ari, Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport 7 (1995) 61–64. CrossrefGoogle Scholar

  • [26] Lecoeur, H., Prevost, M.C. and Gougeon, M.L. Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44 (2001) 65–72. http://dx.doi.org/10.1002/1097-0320(20010501)44:1<65::AID-CYTO1083>3.0.CO;2-QCrossrefGoogle Scholar

  • [27] Alnemri, E.S., Livingston, D.W., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W. and Yuan, J. Human ICE/CED-3 protease nomenclature. Cell 87 (1996) 171. http://dx.doi.org/10.1016/S0092-8674(00)81334-3CrossrefGoogle Scholar

  • [28] Salvesen, G.S. and Dixit, V.M. Caspases: intracellular signaling by proteolysis. Cell 91 (1997) 443–446. http://dx.doi.org/10.1016/S0092-8674(00)80430-4CrossrefGoogle Scholar

  • [29] Lavarik, I.N., Golks, A. and Krammer, P.H. Caspases: pharmacological manipulation of cell death. J. Clin. Invest. 115 (2005) 2665–2672. http://dx.doi.org/10.1172/JCI26252CrossrefGoogle Scholar

  • [30] Yuan, J., Shahan, S., Ledoux, S., Ellis, H.M. and Horvitz, H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta converting enzyme. Cell 75 (1993) 641–652. http://dx.doi.org/10.1016/0092-8674(93)90485-9CrossrefGoogle Scholar

  • [31] Shi, Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 9 (2002) 459–470. http://dx.doi.org/10.1016/S1097-2765(02)00482-3CrossrefGoogle Scholar

  • [32] Yan, N. and Shi, Y. Mechanisms of apoptosis through structural biology. Ann. Rev. Cell Dev. Biol. 21 (2005) 35–56. http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131040CrossrefGoogle Scholar

  • [33] Stennicke, H.R. and Salvesen, G.S. Properties of the caspases. Biochim. Biophys. Acta 1387 (1998) 17–31. Google Scholar

  • [34] Grutter, M.G. Caspases: Key players in programmed cell death. Curr. Opin. Struct. Biol. 10 (2000) 649–655. http://dx.doi.org/10.1016/S0959-440X(00)00146-9CrossrefGoogle Scholar

  • [35] Roth, K.A. Caspases, apoptosis, and Alzheimer’s disease: causation, correlation, and confusion. J. Neuropathol. Exp. Neurol. 60 (2001) 829–838. Google Scholar

  • [36] Cohen, G.M. Caspases: the executioners of apoptosis. Biochem. J. 326 (1997) 1–16. Google Scholar

  • [37] Marshman, E., Ottewell, P.D., Potten, C.S. and Watson, A.J. Caspase activation during spontaneous and radiation-induced apoptosis in the murine intestine. J. Pathol. 195 (2001) 285–292. http://dx.doi.org/10.1002/path.967CrossrefGoogle Scholar

  • [38] Clerk, A., Cole, S.M., Cullingford, T.E., Harrison, J.C., Jormakka, M. and Valks, D.M. Regulation of cardiac myocyte cell death. Pharmacol. Ther. 97 (2003) 223–61. http://dx.doi.org/10.1016/S0163-7258(02)00339-XCrossrefGoogle Scholar

  • [39] Nagata, S. Apoptotic DNA fragmentation. Exp. Cell Res. 256 (2000) 12–18. http://dx.doi.org/10.1006/excr.2000.4834CrossrefGoogle Scholar

  • [40] Earnshaw, W.C., Martins, L.M. and Kaufmann, S.H. Mammalian caspases: Structure, activation, substrates and functions during apoptosis. Ann. Rev. Biochem. 68 (1999) 383–424. http://dx.doi.org/10.1146/annurev.biochem.68.1.383CrossrefGoogle Scholar

  • [41] Liu, X., Kim, C.N., Yang, J., Jemmerson, R. and Wang, X. Induction of apoptosis program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86 (1996) 147–157. http://dx.doi.org/10.1016/S0092-8674(00)80085-9CrossrefGoogle Scholar

  • [42] Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391 (1998) 43–50. http://dx.doi.org/10.1038/34112CrossrefGoogle Scholar

  • [43] Coleman, M.L., Sahai, E.A., Yeo, M., Bosch, M., Dewar, A. and Olson, M.F. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3 (2001) 339–345. http://dx.doi.org/10.1038/35070009CrossrefGoogle Scholar

  • [44] Martinon, F. and Tschopp, J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory disease. Cell 117 (2004) 561–574. http://dx.doi.org/10.1016/j.cell.2004.05.004CrossrefGoogle Scholar

  • [45] Roy, N., Mahadevan, M.S., McLean, M., Shutler, G., Yaraghi, Z., Farahani, R., Baird, S., Benser-Johnson, A., Lefebvre, C., Kang, X., Salih, M., Aubry, H., Tamai, K., Guan, X., Ioannou, P., Crawford, T.O., de Jong, P.J., Surh, L., Ikeda, J.E., Korneluk, R.G. and Mac Kenzie, A. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80 (1995) 167–178. http://dx.doi.org/10.1016/0092-8674(95)90461-1CrossrefGoogle Scholar

  • [46] Cheng, E.H., Levine, B., Boise, L.H., Thompson, C.B. and Hardwick, J.M. Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379 (1996) 554–556. http://dx.doi.org/10.1038/379554a0CrossrefGoogle Scholar

  • [47] Salvesen, G.S. and Duckett, C.S. IAP proteins: blocking the road to death’s door. Nat. Rev. Mol. Cell Biol. 3 (2002) 401–410. http://dx.doi.org/10.1038/nrm830CrossrefGoogle Scholar

  • [48] Deveraux, Q.L. and Reed, J.C. IAP family proteins: suppressors of apoptosis. Genes Dev. 13 (1999) 239–252. CrossrefGoogle Scholar

  • [49] Ekert, P.G., Silke, J. and Vaux, D.L. Caspase inhibitor. Cell Death Differ. 6 (1999) 1081–1086. http://dx.doi.org/10.1038/sj.cdd.4400594CrossrefGoogle Scholar

  • [50] Birnbaum, M.J., Clem, R.J. and Miller, L.K. An apoptosis inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J. Virol. 68 (1994) 2521–2528. Google Scholar

  • [51] Deveraux, Q.L., Takahashi, R., Salvesen, G.S. and Reed, J.C. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388 (1997) 300–304. http://dx.doi.org/10.1038/40901CrossrefGoogle Scholar

  • [52] Deveraux, Q.L., Roy, H.R., Stennicke, H.R., Van Arsdale, T., Zhou, Q., Srinivasula, M., Alnemri, E.S., Salvesen, G.S. and Reed, J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17 (1998) 2215–2223. http://dx.doi.org/10.1093/emboj/17.8.2215CrossrefGoogle Scholar

  • [53] Roy, N., Deveraux, Q.I., Takashashi, R., Salvesen, G.S. and Reed, J.C. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16 (1997) 6914–6925. http://dx.doi.org/10.1093/emboj/16.23.6914CrossrefGoogle Scholar

  • [54] Miller, L.K. An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol. 9 (1999) 323–328. http://dx.doi.org/10.1016/S0962-8924(99)01609-8CrossrefGoogle Scholar

  • [55] Xu, G., Cirilli, M., Huang, Y., Rich, R.L., Myszka, D.G. and Wu, H. Covalent inhibition revealed by the crystal structure of the caspase-8/p35 complex. Nature 410 (2001) 494–497. http://dx.doi.org/10.1038/35068604CrossrefGoogle Scholar

  • [56] Renatus, M., Zhou, Q., Stennicke, H.R., Snipas, S.J., Turk, D., Bankston, L.A., Liddington, R.C. and Salvesen, G.S. Crystal structure of the apoptotic suppressor CrmA in its cleaved form. Structure Fold. Des. 8 (2000) 789–797. http://dx.doi.org/10.1016/S0969-2126(00)00165-9CrossrefGoogle Scholar

  • [57] Sato, T., Irie, S., Krajewski, S. and Reed, J.C. Cloning and sequencing of a cDNA encoding the rat Bcl2 protein. Gene 140 (1994) 291–292. http://dx.doi.org/10.1016/0378-1119(94)90561-4CrossrefGoogle Scholar

  • [58] Adams, J.M. and Cory, S. The Bcl-2 protein family: Arbiters of cell survival. Science 281 (1998) 1322–26. http://dx.doi.org/10.1126/science.281.5381.1322CrossrefGoogle Scholar

  • [59] Burlacu, A. Regulation of apoptosis by Bcl-2 family proteins. J. Cell. Mol. Med. 7 (2003) 249–257. CrossrefGoogle Scholar

  • [60] Tsujimoto, Y., Cossman, J., Jaffe, E. and Croce, C.M. Involvement of the Bcl-2 gene in human follicular lymphoma. Science 228 (1985) 1440–1443. http://dx.doi.org/10.1126/science.3874430CrossrefGoogle Scholar

  • [61] Cory, S. and Adams, J.M. The Bcl2 family: regulators of the cellular life or death switch. Nat. Rev. Cancer 2 (2002) 647–656. http://dx.doi.org/10.1038/nrc883CrossrefGoogle Scholar

  • [62] Puthalakath, H. and Strasser, A. Keeping killers on a tight leash: transcriptional and post-transcriptional control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ. 9 (2002) 505–512. http://dx.doi.org/10.1038/sj.cdd.4400998CrossrefGoogle Scholar

  • [63] Zhu, W., Cowie, A., Wasfy, G.W., Penn, L.Z., Leber, B. and Andrew, D.W. Bcl2 mutants with restricted sub cellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J. 15 (1996) 4130–4141. Google Scholar

  • [64] Griffiths, G.J., Dubrez, L., Morgan, C.P., Jones, N.A., Whitehouse, J., Corfe, B.M., Dive, C. and Hickman, J.A. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in-vivo precede the onset of apoptosis. J. Cell Biol. 144 (1999) 903–914. http://dx.doi.org/10.1083/jcb.144.5.903CrossrefGoogle Scholar

  • [65] Krajewski, S., Tanaka, S., Takayama, S., Schibler, M.J., Fenton, W. and Reed, J.C. Investigation of the Bcl-2 oncoprotein: Residence in the nuclear envelop, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53 (1993) 4701–4714. Google Scholar

  • [66] Nguyen, M., Millar, D.G., Yong, V.W., Korsmeyer, S.J. and Shore, G.C. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268 (1993) 25265–25268. Google Scholar

  • [67] Hussein, M.R., Haemel, A.K. and Wood, G.S. Apoptosis and melanoma: molecular mechanism. J. Pathol. 199 (2003) 275–288. http://dx.doi.org/10.1002/path.1300CrossrefGoogle Scholar

  • [68] Gross, A., Mcdonnell, J.M. and Krosmeyer, S.J. Bcl-2 family members and the mitochondria in apoptosis. Genes Develop. 13 (1999) 1899–1911. Google Scholar

  • [69] Erster, S. and Moll, U.M. Stress induced p53 runs a transcription-independent death program. Biochem. Biophys. Res. Commun. 331 (2005) 843–850. http://dx.doi.org/10.1016/j.bbrc.2005.03.187CrossrefGoogle Scholar

  • [70] Owen-Schaub, L.B., Angelo, L.S., Radinsky, R., Ware, C.F., Gesner, T.G. and Bartos, D.P. Soluble FAS/APO-1 in tumor cells: a potential regulator of apoptosis? Cancer Lett. 94 (1995) 1–8. http://dx.doi.org/10.1016/0304-3835(95)03834-JCrossrefGoogle Scholar

  • [71] Park, D.S., Stefanis, L. and Greene, L.A. Ordering the multiple pathways of apoptosis. Trends Cardiovasc. Med. 7 (1997) 294–299. http://dx.doi.org/10.1016/S1050-1738(97)00090-XCrossrefGoogle Scholar

  • [72] Duensing, A. and Duensing, S. Guilt by association? p53 and development of aneuploidy in cancer. Biochem. Biophys. Res. Commun. 331 (2005) 694–700. http://dx.doi.org/10.1016/j.bbrc.2005.03.157CrossrefGoogle Scholar

  • [73] Aggarwal, B.B. Tumor necrosis factor receptor associated signalling molecules and their role in activation of apoptosis, JNK and NF-kB. Ann. Rheum. Dis. 59 (2000) 6–16. http://dx.doi.org/10.1136/ard.59.suppl_1.i6CrossrefGoogle Scholar

  • [74] Idriss, H.T. and Naismith, J.H. TNF alpha and the TNF receptor super family: structure-function relationship(s). Micro. Res. Tech. 50 (2000) 184–195. http://dx.doi.org/10.1002/1097-0029(20000801)50:3<184::AID-JEMT2>3.0.CO;2-HCrossrefGoogle Scholar

  • [75] MacEwan, D.J. TNF ligands and receptors — a matter of life and death. Br. J. Pharm. 135 (2002) 855–875. http://dx.doi.org/10.1038/sj.bjp.0704549CrossrefGoogle Scholar

  • [76] Wajant, H., Pfizenmaier, K. and Scheurich, P. Tumor necrosis factor signaling. Cell Death Diff. 10 (2003) 45–65. http://dx.doi.org/10.1038/sj.cdd.4401189CrossrefGoogle Scholar

  • [77] Hussein, M.R., Haemel, A.K. and Wood, G.S. p53 related pathways and the molecular pathogenesis of melanoma. Eur. J. Cancer Prev. 12 (2003) 93–100. http://dx.doi.org/10.1097/00008469-200304000-00002CrossrefGoogle Scholar

  • [78] Green, D. and Reed, J. Mitochondria and apoptosis. Science 281 (1998) 1309–1312. http://dx.doi.org/10.1126/science.281.5381.1309CrossrefGoogle Scholar

  • [79] Tsujimoto, Y. and Shimizu, S. The voltage-dependent anion channel: an essential player in apoptosis. Biochimie 84 (2002) 187–193. http://dx.doi.org/10.1016/S0300-9084(02)01370-6CrossrefGoogle Scholar

  • [80] Reed, J.C. Bcl-2 family proteins. Oncogene 17 (1998) 3225–3236. http://dx.doi.org/10.1038/sj.onc.1202591CrossrefGoogle Scholar

  • [81] Shimizu, S., Narita, M. and Tsujimoto, Y. Bcl-2 family protein regulates the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483–487. http://dx.doi.org/10.1038/20959CrossrefGoogle Scholar

  • [82] Ashkenazi, A. and Dixit, V.M. Death receptors: signaling and modulation. Science 281 (1998) 1305–1308. http://dx.doi.org/10.1126/science.281.5381.1305CrossrefGoogle Scholar

  • [83] Schulze-Osthoff, K., Ferrari, D., Los, M., Wesselborg, S. and Peter, M.E. Apoptosis signaling by death receptors. Eur. J. Biochem. 254 (1998) 439–459. http://dx.doi.org/10.1046/j.1432-1327.1998.2540439.xCrossrefGoogle Scholar

  • [84] Peter, M.E. and Krammer, P.H. Mechanisms of CD95 (APO-1/ Fas)-mediated apoptosis. Curr. Opin. Immunol. 10 (1998) 545–551. http://dx.doi.org/10.1016/S0952-7915(98)80222-7CrossrefGoogle Scholar

  • [85] Peter, M.E. and Krammer, P.H. The CD95 (APO-1/ Fas) DISC and beyond. Cell Death Differ. 10 (2003) 26–35. http://dx.doi.org/10.1038/sj.cdd.4401186CrossrefGoogle Scholar

  • [86] Li, H., Zhu, H., Xu, C.J. and Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491–501. http://dx.doi.org/10.1016/S0092-8674(00)81590-1CrossrefGoogle Scholar

  • [87] Luo, X., Budihardjo, I., Zou, H., Slaughter, C. and Wang, X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94 (1998) 481–490. http://dx.doi.org/10.1016/S0092-8674(00)81589-5CrossrefGoogle Scholar

  • [88] Chaudhary, P.M., Eby, M., Jasmin, A., Bookwalter, A., Murray, J. and Hood, L. Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappa B pathway. Immunity 7 (1997) 821–830. http://dx.doi.org/10.1016/S1074-7613(00)80400-8Google Scholar

  • [89] Stennicke, H.R., Jurgensmeier, J.M., Shin, H., Deveraux, Q., Wolf, B.B., Yang, X., Zhou, Q., Ellerby, H.M., Ellerby, L.M., Bredesen, D., Green, D.R., Reed, J.C., Froelich, C.J. and Salvesen, G. S. Procaspase-3 is a major physiologic target of caspase-8. J. Biol. Chem. 273 (1998) 27084–27090. http://dx.doi.org/10.1074/jbc.273.42.27084Google Scholar

  • [90] Scaffidi, C., Schmitz, I., Krammer, P.H. and Peter, M.E. The role of c-FLIP in modulation of CD95 induced apoptosis. J. Biol. Chem. 274 (1999) 1541–1548. http://dx.doi.org/10.1074/jbc.274.3.1541CrossrefGoogle Scholar

  • [91] Golks, A., Brenner, D., Fritsch, C., Krammer, P.H. and Lavrik, L.N. cFLIPR: a new regulator of death receptor-induced apoptosis. J. Biol. Chem. 280 (2005) 14507–14513. http://dx.doi.org/10.1074/jbc.M414425200CrossrefGoogle Scholar

  • [92] Harris, S.L. and Levine, A.J. The p53 pathway: positive and negative feed back loops. Oncogene 24 (2005) 2899–2908. http://dx.doi.org/10.1038/sj.onc.1208615CrossrefGoogle Scholar

  • [93] Li, F., Srinivasam, A., Wang, Y., Armstrong, R.C., Tomaselli, K.J. and Fritz, L.C. Cell-specific induction of apoptosis by microinjection of cytochrome c. J. Biol. Chem. 272 (1997) 30299–30305. http://dx.doi.org/10.1074/jbc.272.48.30299CrossrefGoogle Scholar

  • [94] Hengartner, M.O. The biochemistry of apoptosis. Nature 407 (2000) 770–776. http://dx.doi.org/10.1038/35037710CrossrefGoogle Scholar

  • [95] Xu, C., Bailly-Maitre, B. and Reed, J.C. Endoplasmic reticulam stress: cell life and death decisions. J. Clin. Invest. 115 (2005) 2656–2664. http://dx.doi.org/10.1172/JCI26373CrossrefGoogle Scholar

  • [96] Hick, S.W. and Machamer, C.E. Golgi structure in stress sensing and apoiptosis. Biochem. Biophys. Acta 1744 (2005) 406–414. http://dx.doi.org/10.1016/j.bbamcr.2005.03.002CrossrefGoogle Scholar

  • [97] Wu, Y., Tibrewal, N. and Brige, R.B. Phospohatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. 16 (2006) 189–197. http://dx.doi.org/10.1016/j.tcb.2006.02.003CrossrefGoogle Scholar

  • [98] Savill, J. Recognition and phagocytosis of cells undergoing apoptosis. Br. Med. Bull. 53 (1997) 491–508. CrossrefGoogle Scholar

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Published Online: 2006-09-05

Published in Print: 2006-12-01


Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-006-0041-3.

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[31]
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[42]
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[43]
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[46]
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[47]
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[48]
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[49]
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[50]
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[51]
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[52]
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[53]
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[54]
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[55]
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[56]
Karola Wittig, Jennifer Kasper, Stefanie Seipp, and Thomas Leitz
Zoology, 2011, Volume 114, Number 1, Page 11
[57]
Louis P. Sandjo, Vincent Rincheval, Bonaventure T. Ngadjui, and Gilbert Kirsch
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[58]
Indrajit Chowdhury, Binu Tharakan, and Ganapathy K. Bhat
Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2008, Volume 151, Number 1, Page 10
[60]
A. V. Sirotkin, A. Benčo, A. Tandlmajerová, and D. Vašíček
Cell Proliferation, 2012, Volume 45, Number 1, Page 9
[61]
Cheol Park, Hee Jae Shin, Gi-Young Kim, Taeg Kyu Kwon, Taek-Jeong Nam, Se-Kwon Kim, Jaehun Cheong, Il-Whan Choi, and Yung Hyun Choi
Toxicology in Vitro, 2008, Volume 22, Number 6, Page 1573
[62]
Helle Evi Simovart, Andres Arend, Jüri Lieberg, and Marina Aunapuu
International Journal of Vascular Medicine, 2011, Volume 2011, Page 1
[63]
Huang Chun, Wu Hao, Zhang Honghai, Li Ning, Wu Yasong, and Dexi Chen
Brain Research, 2009, Volume 1257, Page 75
[64]
C. Schmidt, M. Fronza, M. Goettert, F. Geller, S. Luik, E.M.M. Flores, C.F. Bittencourt, G.D. Zanetti, B.M. Heinzmann, S. Laufer, and I. Merfort
Journal of Ethnopharmacology, 2009, Volume 122, Number 3, Page 523
[65]
Sodhi K. Rupinder, Aulakh K. Gurpreet, and Singh Manjeet
Vascular Pharmacology, 2007, Volume 46, Number 6, Page 383
[66]
I. Lengwehasatit, A. Nuchtas, S. Tungpradabkul, S. Sirisinha, and P. Utaisincharoen
Microbial Pathogenesis, 2008, Volume 44, Number 3, Page 238
[67]
Ana Rita S. Coutinho, Mayra E.O. Assumpção, and Vilceu Bordignon
Molecular Reproduction and Development, 2011, Volume 78, Number 9, Page 673
[68]
Sónia C.P. Costa, Carolina Varela Chavez, Grégory Jubelin, Alain Givaudan, Jean-Michel Escoubas, Michel Brehélin, and Robert Zumbihl
Microbes and Infection, 2010, Volume 12, Number 3, Page 182
[69]
David B. Rivers, Fevzi Uçkan, Ekrem Ergin, and Donald A. Keefer
Journal of Insect Physiology, 2010, Volume 56, Number 12, Page 1935
[70]
Nashmil Emami and Eleftherios P. Diamandis
Molecular Oncology, 2007, Volume 1, Number 3, Page 269
[71]
Indrajit Chowdhury, Alicia Branch, Moshood Olatinwo, Kelwyn Thomas, Roland Matthews, and Winston E. Thompson
Life Sciences, 2011, Volume 89, Number 9-10, Page 295
[72]
Elzbieta Kolaczkowska, Agnieszka Koziol, Barbara Plytycz, Bernd Arnold, and Ghislain Opdenakker
Immunology Letters, 2009, Volume 126, Number 1-2, Page 73
[73]
Isabella Savini, Rosaria Arnone, Maria Valeria Catani, and Luciana Avigliano
Nutrition and Cancer, 2009, Volume 61, Number 3, Page 381
[74]
Ujwal J. Pyati, A. Thomas Look, and Matthias Hammerschmidt
Seminars in Cancer Biology, 2007, Volume 17, Number 2, Page 154
[75]
Udi Zelig, Joseph Kapelushnik, Raymond Moreh, Shaul Mordechai, and Ilana Nathan
Biophysical Journal, 2009, Volume 97, Number 7, Page 2107
[76]
Ji-Young Lim, Yae-Lim Lee, Hae-Rin Lee, Woo-Young Choi, Won-Ho Lee, and Yung-Hyun Choi
Toxicological Research, 2007, Volume 23, Number 3, Page 215
[77]
Pappanaicken R. Kumaresan, Yan Wang, Mary Saunders, Yoshiko Maeda, Ruiwu Liu, Xiaobing Wang, and Kit Sang Lam
ACS Combinatorial Science, 2011, Volume 13, Number 3, Page 259
[78]
Eva Karamitopoulou, Cyrill A. Rentsch, Regula Markwalder, Claudio Vallan, George N. Thalmann, and Thomas Brunner
Pathology, 2010, Volume 42, Number 1, Page 37
[79]
Mike-Andrew Westhoff and Simone Fulda
Drug Resistance Updates, 2009, Volume 12, Number 4-5, Page 127
[80]
LiShun Wang and GuoQiang Chen
Science China Life Sciences, 2011, Volume 54, Number 3, Page 209
[81]
Stephanie L. Lomonaco, Xiaoxin S. Xu, and Gan Wang
DNA and Cell Biology, 2009, Volume 28, Number 6, Page 285
[82]
Ilse Kranner, Hongying Chen, Hugh W. Pritchard, Stephen R. Pearce, and Simona Birtić
Plant Growth Regulation, 2011, Volume 63, Number 1, Page 63
[83]
F Gonzalvez and A Ashkenazi
Oncogene, 2010, Volume 29, Number 34, Page 4752
[84]
David M. Conrad, Suzanne J. Furlong, Carolyn D. Doucette, Kenneth A. West, and David W. Hoskin
Apoptosis, 2010, Volume 15, Number 5, Page 597
[85]
Margherita Lasi, Charles N. David, and Angelika Böttger
Apoptosis, 2010, Volume 15, Number 3, Page 269
[86]
Leigh Ann Callahan and Gerald S. Supinski
Critical Care Medicine, 2009, Volume 37, Page S354
[87]
A. D. Amsel, M. Rathaus, N. Kronman, and H. Y. Cohen
Proceedings of the National Academy of Sciences, 2008, Volume 105, Number 13, Page 5117
[88]
S. Jin, Q. Y. Zhang, X. M. Kang, J. X. Wang, and W. H. Zhao
Annals of Oncology, 2010, Volume 21, Number 2, Page 263
[89]
P. K. Kreeger and D. A. Lauffenburger
Carcinogenesis, 2010, Volume 31, Number 1, Page 2
[90]
D. Han, Y. Ding, S.-L. Liu, G. Wang, I.-C. Si, X. Wang, L. Cui, and D. Huang
Acta Biochimica et Biophysica Sinica, 2009, Volume 41, Number 11, Page 938
[91]
Mathieu Toumi, Vincent Rincheval, Ashley Young, Danielle Gergeres, Edward Turos, François Couty, Bernard Mignotte, and Gwilherm Evano
European Journal of Organic Chemistry, 2009, Volume 2009, Number 20, Page 3368
[92]
Hiroaki Inaba, Masae Kuboniwa, Brian Bainbridge, Özlem Yilmaz, Joseph Katz, Kathleen T. Shiverick, Atsuo Amano, and Richard J. Lamont
Cellular Microbiology, 2009, Volume 11, Number 10, Page 1517
[93]
Jean Lud Cadet, Irina N. Krasnova, Subramaniam Jayanthi, and Johnalyn Lyles
Neurotoxicity Research, 2007, Volume 11, Number 3-4, Page 183
[94]
B. Hübner, H. Strickfaden, S. Müller, M. Cremer, and T. Cremer
European Biophysics Journal, 2009, Volume 38, Number 6, Page 729
[95]
Pablo E. Vivas-Mejía, Bulent Ozpolat, Xian Chen, and Gabriel Lopez-Berestein
International Journal of Cancer, 2009, Volume 125, Number 2, Page 264
[96]
Mehmet Kemal Tur, Inga Neef, Edgar Jost, Oliver Galm, Gernot Jäger, Michael Stöcker, Markus Ribbert, Rainhardt Osieka, Uwe Klinge, and Stefan Barth
Journal of Immunotherapy, 2009, Volume 32, Number 5, Page 431
[97]
Alexander V. Sirotkin, Dmitriy Ovcharenko, Andrej Benčo, and Miloš Mlynček
Functional & Integrative Genomics, 2009, Volume 9, Number 2, Page 185
[98]
A. Zuppini, C. Andreoli, and B. Baldan
Plant and Cell Physiology, 2007, Volume 48, Number 7, Page 1000
[99]
Avi Ashkenazi
Nature Reviews Drug Discovery, 2008, Volume 7, Number 12, Page 1001
[100]
Frank Wehner, Andrea Nören-Müller, Oliver Müller, Ivan Reis-Corrêa, Athanassios Giannis, and Herbert Waldmann
ChemBioChem, 2008, Volume 9, Number 3, Page 401
[101]
H. Takle and Ø. Andersen
Journal of Fish Biology, 2007, Volume 71, Number sc, Page 326

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