Current concepts in apoptosis: The physiological suicide program revisited : Cellular and Molecular Biology Letters Jump to ContentJump to Main Navigation
Show Summary Details

Cellular and Molecular Biology Letters

Editor-in-Chief: /


IMPACT FACTOR increased in 2015: 1.753

SCImago Journal Rank (SJR) 2015: 0.788
Source Normalized Impact per Paper (SNIP) 2015: 0.645
Impact per Publication (IPP) 2015: 1.748

99,00 € / $149.00 / £75.00*

Online
ISSN
1689-1392
See all formats and pricing



Select Volume and Issue
Loading journal volume and issue information...

Current concepts in apoptosis: The physiological suicide program revisited

1Department of Obstetrics and Gynecology, Morehouse School of Medicine, Atlanta, GA, USA

2Department of Neurology, Scott and White Clinic, The Texas A & M University Health Science Center, College of Medicine, Temple, Texas, USA

© 2006 University of Wrocław, Poland. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Citation Information: Cellular and Molecular Biology Letters. Volume 11, Issue 4, Pages 506–525, ISSN (Online) 1689-1392, DOI: 10.2478/s11658-006-0041-3, September 2006

Publication History

Published Online:
2006-09-05

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)80564-4 [CrossRef]

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

  • [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.1711050103 [CrossRef]

  • [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. [CrossRef]

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

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

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

  • [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)00046-7 [CrossRef]

  • [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.14.2.133 [CrossRef]

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

  • [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.93.6.2239 [CrossRef]

  • [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/JCI26390 [CrossRef]

  • [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/BF00174615 [CrossRef]

  • [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.4400852 [CrossRef]

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

  • [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-04-2223 [CrossRef]

  • [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.1207528 [CrossRef]

  • [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)80088-3 [CrossRef]

  • [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:1012159208559 [CrossRef]

  • [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.1994.1184 [CrossRef]

  • [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)88932-1 [CrossRef]

  • [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-G [CrossRef]

  • [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-I [CrossRef]

  • [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.119.3.493 [CrossRef]

  • [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. [CrossRef]

  • [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-Q [CrossRef]

  • [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)81334-3 [CrossRef]

  • [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)80430-4 [CrossRef]

  • [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/JCI26252 [CrossRef]

  • [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)90485-9 [CrossRef]

  • [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)00482-3 [CrossRef]

  • [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.21.012704.131040 [CrossRef]

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

  • [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)00146-9 [CrossRef]

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

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

  • [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.967 [CrossRef]

  • [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-X [CrossRef]

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

  • [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.68.1.383 [CrossRef]

  • [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)80085-9 [CrossRef]

  • [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/10.1038/34112 [CrossRef]

  • [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/10.1038/35070009 [CrossRef]

  • [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.2004.05.004 [CrossRef]

  • [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)90461-1 [CrossRef]

  • [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/10.1038/379554a0 [CrossRef]

  • [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/nrm830 [CrossRef]

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

  • [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.4400594 [CrossRef]

  • [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.

  • [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/10.1038/40901 [CrossRef]

  • [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/17.8.2215 [CrossRef]

  • [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/16.23.6914 [CrossRef]

  • [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)01609-8 [CrossRef]

  • [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/10.1038/35068604 [CrossRef]

  • [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)00165-9 [CrossRef]

  • [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)90561-4 [CrossRef]

  • [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.281.5381.1322 [CrossRef]

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

  • [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.3874430 [CrossRef]

  • [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/nrc883 [CrossRef]

  • [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.4400998 [CrossRef]

  • [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.

  • [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.144.5.903 [CrossRef]

  • [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.

  • [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.

  • [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.1300 [CrossRef]

  • [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.

  • [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.2005.03.187 [CrossRef]

  • [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-J [CrossRef]

  • [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-X [CrossRef]

  • [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.2005.03.157 [CrossRef]

  • [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.i6 [CrossRef]

  • [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-H [CrossRef]

  • [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.0704549 [CrossRef]

  • [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.4401189 [CrossRef]

  • [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/10.1097/00008469-200304000-00002 [CrossRef]

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

  • [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)01370-6 [CrossRef]

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

  • [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/10.1038/20959 [CrossRef]

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

  • [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.x [CrossRef]

  • [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)80222-7 [CrossRef]

  • [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.4401186 [CrossRef]

  • [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)81590-1 [CrossRef]

  • [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)81589-5 [CrossRef]

  • [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)80400-8

  • [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.273.42.27084

  • [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.274.3.1541 [CrossRef]

  • [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.M414425200 [CrossRef]

  • [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.1208615 [CrossRef]

  • [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.272.48.30299 [CrossRef]

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

  • [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/JCI26373 [CrossRef]

  • [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.2005.03.002 [CrossRef]

  • [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.2006.02.003 [CrossRef]

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

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Rakesh Kumar, Shailesh Kumar Pate, B.V. Rami Reddy, Mukesh Bhatt, K. Karthik, Ravi Kumar Gandham, Yashpal Singh Mali, and Kuldeep Dhama
Asian Journal of Animal and Veterinary Advances, 2015, Volume 10, Number 10, Page 646
[2]
Mohd. Akhlakur Rahman, Mutsunori Shirai, Md. Abdul Aziz, Rie Ushirokita, Sayuri Kubota, Harumi Suzuki, and Yoshinao Azuma
Apoptosis, 2015
[3]
Letteria Minutoli, Salvatore Arena, Pietro Antonuccio, Carmelo Romeo, Alessandra Bitto, Carlo Magno, Mariagrazia Rinaldi, Antonio Micali, Natasha Irrera, Gabriele Pizzino, Federica Galfo, Francesco Squadrito, Domenica Altavilla, and Herbert Marini
BioMed Research International, 2015, Volume 2015, Page 1
[4]
Yanfeng Gao, Xiongwei Huo, Liu Dong, Xuejun Sun, He Sai, Guangbing Wei, Yizhuang Xu, Yuanfu Zhang, and Jinguang Wu
Molecular Medicine Reports, 2014
[5]
Sijun Deng, Shusheng Tang, Shen Zhang, Chaoming Zhang, Congcong Wang, Yan Zhou, Chongshan Dai, and Xilong Xiao
Food and Chemical Toxicology, 2015, Volume 75, Page 173
[6]
Constant Pieme, Guru Santosh, Emmanuel Tekwu, Tülin Askun, Hatice Aydeniz, Jeanne Ngogang, Shashi Bhushan, and Ajit Saxena
Biological Research, 2014, Volume 47, Number 1, Page 54
[7]
Varda Shoshan-Barmatz, Danya Ben-Hail, Lee Admoni, Yakov Krelin, and Shambhoo Sharan Tripathi
Biochimica et Biophysica Acta (BBA) - Biomembranes, 2014
[8]
J.K.F. Wong, S. Alyouha, K.E. Kadler, M.W.J. Ferguson, and D.A. McGrouther
Matrix Biology, 2010, Volume 29, Number 6, Page 525
[9]
Chia-Jung Li, Shih-Fang Tsang, Chun-Hao Tsai, Hsin-Yi Tsai, Jong-Ho Chyuan, and Hsue-Yin Hsu
Evidence-Based Complementary and Alternative Medicine, 2012, Volume 2012, Page 1
[11]
Shuo Yang, Liming Wang, and Qingbo Kong
Cell Biochemistry and Biophysics, 2014, Volume 70, Number 2, Page 765
[12]
Indrajit Chowdhury, Winston E. Thompson, and Kelwyn Thomas
Journal of Cellular Physiology, 2014, Volume 229, Number 8, Page 998
[13]
Shan Miao, Xiaopeng Shi, Hai Zhang, Siwang Wang, Jiyuan Sun, Wei Hua, Qing Miao, Yong Zhao, and Caiqin Zhang
International Journal of Molecular Sciences, 2011, Volume 12, Number 12, Page 3831
[14]
Gi-Young Kim, Wun-Jae Kim, and Yung Hyun Choi
Marine Drugs, 2011, Volume 9, Number 12, Page 2176
[15]
A V Sirotkin, A Benco, A Tandlmajerova, D Vasicek, J Kotwica, K Darlak, and F Valenzuela
Reproduction, 2008, Volume 136, Number 5, Page 611
[16]
C. D. Bortner and J. A. Cidlowski
Philosophical Transactions of the Royal Society B: Biological Sciences, 2014, Volume 369, Number 1638, Page 20130104
[17]
Yue Xu, Shanshan Yu, Qinmeng Shu, Lu Yang, Cheng Yang, Jiawei Wang, Fan Xu, Min Ji, and Xiaoling Liang
Journal of Molecular Neuroscience, 2014, Volume 52, Number 3, Page 331
[18]
Indrajit Chowdhury, Winston E. Thompson, Crystal Welch, Kelwyn Thomas, and Roland Matthews
Apoptosis, 2013, Volume 18, Number 12, Page 1513
[19]
Jialiang Wang, Jianing Zu, Gongping Xu, Wei Zhao, and Yan Jinglong
Tumor Biology, 2014, Volume 35, Number 2, Page 1551
[20]
Sijun Deng, Hui Yuan, Jine Yi, Yin Lu, Qiang Wei, Chengzhi Guo, Jing Wu, Liyun Yuan, and Zuping He
Journal of Veterinary Science, 2013, Volume 14, Number 3, Page 281
[21]
Lingxin Zhu, Jingwen Yang, Jie Zhang, and Bin Peng
Journal of Endodontics, 2013, Volume 39, Number 11, Page 1379
[22]
George S Krasnov, Alexey A Dmitriev, Valentina A Lakunina, Alexander A Kirpiy, and Anna V Kudryavtseva
Expert Opinion on Therapeutic Targets, 2013, Volume 17, Number 10, Page 1221
[23]
Rajesh S. Alphonse, Arul Vadivel, Lavinia Coltan, Farah Eaton, Amy J. Barr, Jason R. B. Dyck, and Bernard Thébaud
American Journal of Respiratory Cell and Molecular Biology, 2011, Volume 44, Number 2, Page 146
[25]
Milena Petriccione, Valentina Forte, Diego Valente, and Claudia Ciniglia
Environmental Science and Pollution Research, 2013, Volume 20, Number 7, Page 4859
[26]
Juan I. Barrasa, Nieves Olmo, Ma Antonia Lizarbe, and Javier Turnay
Toxicology in Vitro, 2013, Volume 27, Number 2, Page 964
[27]
Tahany M. Shams, Maha M. Atwa, and Mohamed E. Shams
Egyptian Journal of Pathology, 2012, Volume 32, Number 1, Page 68
[28]
Jiyou Li, Qingfeng Meng, Yu Sun, and Huadong Qing
Molecular Biology Reports, 2013, Volume 40, Number 1, Page 401
[29]
You-Cheng Hseu, Hsiao-Tung Tsou, K. J. Senthil Kumar, Kai-Yuan Lin, Hsueh-Wei Chang, and Hsin-Ling Yang
Evidence-Based Complementary and Alternative Medicine, 2012, Volume 2012, Page 1
[30]
A. Scislowska-Czarnecka, E. Pamula, A. Tlalka, and E. Kolaczkowska
Journal of Biomaterials Science, Polymer Edition, 2012, Volume 23, Number 6, Page 715
[31]
Guangfeng Li, Anne Gleinich, Helene Lau, and Martina Zimmermann
Neurochemistry International, 2012, Volume 61, Number 7, Page 1011
[32]
Mi Na Kim, Kyung Eun Lee, Jung Yeon Hong, Won Il Heo, Kyung Won Kim, Kyu Earn Kim, and Myung Hyun Sohn
Biochemical and Biophysical Research Communications, 2012, Volume 421, Number 4, Page 790
[33]
Qingfeng Meng, Jia Lv, Hongyan Ge, Lu Zhang, Fei Xue, Yuanmao Zhu, and Ping Liu
Molecular Biology Reports, 2012, Volume 39, Number 5, Page 5867
[34]
Kunga Mohan Ramkumar, Chinnasamy Manjula, Georgepeter GnanaKumar, Muzafar A. Kanjwal, Thillai V. Sekar, Ramasamy Paulmurugan, and Palanisamy Rajaguru
European Journal of Pharmaceutics and Biopharmaceutics, 2012, Volume 81, Number 2, Page 324
[35]
Hajer Taga, Yves Chilliard, Bruno Meunier, Christophe Chambon, Brigitte Picard, Maria C. Zingaretti, Saverio Cinti, and Muriel Bonnet
Journal of Cellular Physiology, 2012, Volume 227, Number 4, Page 1688
[36]
Karola Wittig, Jennifer Kasper, Stefanie Seipp, and Thomas Leitz
Zoology, 2011, Volume 114, Number 1, Page 11
[38]
A. V. Sirotkin, A. Benčo, A. Tandlmajerová, and D. Vašíček
Cell Proliferation, 2012, Volume 45, Number 1, Page 9
[39]
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
[40]
Helle Evi Simovart, Andres Arend, Jüri Lieberg, and Marina Aunapuu
International Journal of Vascular Medicine, 2011, Volume 2011, Page 1
[41]
Huang Chun, Wu Hao, Zhang Honghai, Li Ning, Wu Yasong, and Dexi Chen
Brain Research, 2009, Volume 1257, Page 75
[42]
Sodhi K. Rupinder, Aulakh K. Gurpreet, and Singh Manjeet
Vascular Pharmacology, 2007, Volume 46, Number 6, Page 383
[43]
I. Lengwehasatit, A. Nuchtas, S. Tungpradabkul, S. Sirisinha, and P. Utaisincharoen
Microbial Pathogenesis, 2008, Volume 44, Number 3, Page 238
[44]
Ana Rita S. Coutinho, Mayra E.O. Assumpção, and Vilceu Bordignon
Molecular Reproduction and Development, 2011, Volume 78, Number 9, Page 673
[45]
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
[46]
David B. Rivers, Fevzi Uçkan, Ekrem Ergin, and Donald A. Keefer
Journal of Insect Physiology, 2010, Volume 56, Number 12, Page 1935
[47]
Nashmil Emami and Eleftherios P. Diamandis
Molecular Oncology, 2007, Volume 1, Number 3, Page 269
[48]
Indrajit Chowdhury, Alicia Branch, Moshood Olatinwo, Kelwyn Thomas, Roland Matthews, and Winston E. Thompson
Life Sciences, 2011, Volume 89, Number 9-10, Page 295
[49]
Elzbieta Kolaczkowska, Agnieszka Koziol, Barbara Plytycz, Bernd Arnold, and Ghislain Opdenakker
Immunology Letters, 2009, Volume 126, Number 1-2, Page 73
[50]
Isabella Savini, Rosaria Arnone, Maria Valeria Catani, and Luciana Avigliano
Nutrition and Cancer, 2009, Volume 61, Number 3, Page 381
[51]
Ujwal J. Pyati, A. Thomas Look, and Matthias Hammerschmidt
Seminars in Cancer Biology, 2007, Volume 17, Number 2, Page 154
[52]
Udi Zelig, Joseph Kapelushnik, Raymond Moreh, Shaul Mordechai, and Ilana Nathan
Biophysical Journal, 2009, Volume 97, Number 7, Page 2107
[53]
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
[54]
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
[55]
Eva Karamitopoulou, Cyrill A. Rentsch, Regula Markwalder, Claudio Vallan, George N. Thalmann, and Thomas Brunner
Pathology, 2010, Volume 42, Number 1, Page 37
[56]
Mike-Andrew Westhoff and Simone Fulda
Drug Resistance Updates, 2009, Volume 12, Number 4-5, Page 127
[57]
LiShun Wang and GuoQiang Chen
Science China Life Sciences, 2011, Volume 54, Number 3, Page 209
[58]
Stephanie L. Lomonaco, Xiaoxin S. Xu, and Gan Wang
DNA and Cell Biology, 2009, Volume 28, Number 6, Page 285
[59]
Ilse Kranner, Hongying Chen, Hugh W. Pritchard, Stephen R. Pearce, and Simona Birtić
Plant Growth Regulation, 2011, Volume 63, Number 1, Page 63
[60]
F Gonzalvez and A Ashkenazi
Oncogene, 2010, Volume 29, Number 34, Page 4752
[61]
David M. Conrad, Suzanne J. Furlong, Carolyn D. Doucette, Kenneth A. West, and David W. Hoskin
Apoptosis, 2010, Volume 15, Number 5, Page 597
[62]
Margherita Lasi, Charles N. David, and Angelika Böttger
Apoptosis, 2010, Volume 15, Number 3, Page 269
[63]
Leigh Ann Callahan and Gerald S. Supinski
Critical Care Medicine, 2009, Volume 37, Page S354
[64]
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
[65]
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
[66]
P. K. Kreeger and D. A. Lauffenburger
Carcinogenesis, 2010, Volume 31, Number 1, Page 2
[67]
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
[68]
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
[69]
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
[70]
Jean Lud Cadet, Irina N. Krasnova, Subramaniam Jayanthi, and Johnalyn Lyles
Neurotoxicity Research, 2007, Volume 11, Number 3-4, Page 183
[71]
B. Hübner, H. Strickfaden, S. Müller, M. Cremer, and T. Cremer
European Biophysics Journal, 2009, Volume 38, Number 6, Page 729
[72]
Pablo E. Vivas-Mejía, Bulent Ozpolat, Xian Chen, and Gabriel Lopez-Berestein
International Journal of Cancer, 2009, Volume 125, Number 2, Page 264
[73]
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
[74]
Alexander V. Sirotkin, Dmitriy Ovcharenko, Andrej Benčo, and Miloš Mlynček
Functional & Integrative Genomics, 2009, Volume 9, Number 2, Page 185
[75]
A. Zuppini, C. Andreoli, and B. Baldan
Plant and Cell Physiology, 2007, Volume 48, Number 7, Page 1000
[76]
Avi Ashkenazi
Nature Reviews Drug Discovery, 2008, Volume 7, Number 12, Page 1001
[77]
Frank Wehner, Andrea Nören-Müller, Oliver Müller, Ivan Reis-Corrêa, Athanassios Giannis, and Herbert Waldmann
ChemBioChem, 2008, Volume 9, Number 3, Page 401
[78]
H. Takle and Ø. Andersen
Journal of Fish Biology, 2007, Volume 71, Number sc, Page 326

Comments (0)

Please log in or register to comment.