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Department of Physiology and the Lineberger Comprehensive Cancer Research Center Cell Biology Program, University of North Carolina at Chapel Hill Chapel Hill, North Carolina 27599
Correspondence: Address requests for reprints to: John A. Cidlowski, Ph.D., Department of Physiology, CB 7545, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599.
Abstract
I. Introduction: DEATH, along with growth and differentiation, is a critical part of the life cycle of a cell. Homeostatic control of cell number is thought to be the result of the dynamic balance between cell proliferation and cell death. It is only in the past few years, however, that attention has been focused on the physiological occurrence of cell death and its role in homeostasis. Researchers have become increasingly more aware during this time that this type of "natural" death, which is now called apoptosis or programmed cell death, is a widespread phenomenon that plays a crucial role in a myriad of physiological and pathological processes. This review first briefly covers some historical perspective on the discovery of apoptotic cell death, the characteristic morphology that accompanies this process, and the numerous cell types and mediators with which programmed cell death is associated. The bulk of the review discusses our current understanding of the biochemical and molecular mechanisms by which apoptosis occurs. Finally, the potential for therapeutic uses of apoptosis is discussed, along with some comments on the physiological importance of programmed cell death and where the future lies for this quickly expanding and exciting field.
Footnotes
* This work was supported by National Institutes of Health Grant DK-32078.
Present Address: Carnegie Institution of Washington, Department of Embryology, 115 West University Parkway, Baltimore, Maryland, 21210.
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A. G. Yakovlev, S. M. Knoblach, L. Fan, G. B. Fox, R. Goodnight, and A. I. Faden Activation of CPP32-Like Caspases Contributes to Neuronal Apoptosis and Neurological Dysfunction after Traumatic Brain Injury J. Neurosci., October 1, 1997; 17(19): 7415 - 7424. [Abstract] [Full Text] [PDF]
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 S. Taga, K. Carlier, Z. Mishal, C. Capoulade, M. Mangeney, Y. Lecluse, D. Coulaud, C. Tetaud, L. L. Pritchard, T. Tursz, et al. Intracellular Signaling Events in CD77-Mediated Apoptosis of Burkitt's Lymphoma Cells Blood, October 1, 1997; 90(7): 2757 - 2767. [Abstract] [Full Text] [PDF]
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 G. F. Erickson Defining Apoptosis: Players and Systems Reproductive Sciences, September 1, 1997; 4(5): 219 - 228. [Abstract] [PDF]
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 S. S. Mpoke and J. Wolfe Differential Staining of Apoptotic Nuclei in Living Cells: Application to Macronuclear Elimination in Tetrahymena J. Histochem. Cytochem., May 1, 1997; 45(5): 675 - 684. [Abstract] [Full Text] [PDF]
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B. C. J. M. Fauser and A. M. van Heusden Manipulation of Human Ovarian Function: Physiological Concepts and Clinical Consequences Endocr. Rev., February 1, 1997; 18(1): 71 - 106. [Abstract] [Full Text]
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 I. Escargueil-Blanc, O. Meilhac, M.-T. Pieraggi, J.-F. Arnal, R. Salvayre, and A. Negre-Salvayre Oxidized LDLs Induce Massive Apoptosis of Cultured Human Endothelial Cells Through a Calcium-Dependent Pathway: Prevention by Aurintricarboxylic Acid Arterioscler Thromb Vasc Biol, February 1, 1997; 17(2): 331 - 339. [Abstract] [Full Text]
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 R Mittler, L Simon, and E Lam Pathogen-induced programmed cell death in tobacco J. Cell Sci., January 6, 1997; 110(11): 1333 - 1344. [Abstract] [PDF]
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A. Hurwitz, K. Ruutiainen-Altman, L. Marzella, L. Botero, M. Dushnik, and E. Y. Adashi Follicular Atresia as an Apoptotic Process: Atresia-Associated Increase in the Ovarian Expression of the Putative Apoptotic Marker Sulfated Glycoprotein-2 Reproductive Sciences, July 1, 1996; 3(4): 199 - 208. [Abstract] [PDF]
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M. Fraser, S. Tynan, A Papaioannou, C. Ireland, and S. Pittman Endo-exonuclease of human leukaemic cells: evidence for a role in apoptosis J. Cell Sci., January 9, 1996; 109(9): 2343 - 2360. [Abstract] [PDF]
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T Furuchi, K Masuko, Y Nishimune, M Obinata, and Y Matsui Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia Development, January 6, 1996; 122(6): 1703 - 1709. [Abstract] [PDF]
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A. Torriglia, E. Chaudun, F.ço. Chany-Fournier, J.-C. Jeanny, Y. Courtois, and M.-F. Counis Involvement of DNase II in Nuclear Degeneration during Lens Cell Differentiation J. Biol. Chem., December 1, 1995; 270(48): 28579 - 28585. [Abstract] [Full Text] [PDF]
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 C.-J. Chang, W. W. Lai, D. P. Edward, and M. O. M. Tso Apoptotic Photoreceptor Cell Death After Traumatic Retinal Detachment in Humans Arch Ophthalmol, July 1, 1995; 113(7): 880 - 886. [Abstract] [PDF]
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A. Palumbo and J. Yeh Apoptosis as a Basic Mechanism in the Ovarian Cycle: Folicular Atresia and Luteal Regression Reproductive Sciences, May 1, 1995; 2(3): 565 - 573. [Abstract] [PDF]
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M. J. Jones and A. W. Murray Evidence That Ceramide Selectively Inhibits Protein Kinase C-alpha Translocation and Modulates Bradykinin Activation of Phospholipase D J. Biol. Chem., March 10, 1995; 270(10): 5007 - 5013. [Abstract] [Full Text] [PDF]
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K Herrup and J. Busser The induction of multiple cell cycle events precedes target-related neuronal death Development, January 8, 1995; 121(8): 2385 - 2395. [Abstract] [PDF]
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J. Tidball, D. Albrecht, B. Lokensgard, and M. Spencer Apoptosis precedes necrosis of dystrophin-deficient muscle J. Cell Sci., January 6, 1995; 108(6): 2197 - 2204. [Abstract] [PDF]
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 K A Howes, N Ransom, D S Papermaster, J G Lasudry, D M Albert, and J J Windle Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes & Dev., June 1, 1994; 8(11): 1300 - 1310. [Abstract] [PDF]
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B. Gjertsen, L. Cressey, S Ruchaud, G Houge, M Lanotte, and S. Doskeland Multiple apoptotic death types triggered through activation of separate pathways by cAMP and inhibitors of protein phosphatases in one (IPC leukemia) cell line J. Cell Sci., January 12, 1994; 107(12): 3363 - 3377. [Abstract] [PDF]
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G. Bicknell, R. Snowden, and G. Cohen Formation of high molecular mass DNA fragments is a marker of apoptosis in the human leukaemic cell line, U937 J. Cell Sci., January 9, 1994; 107(9): 2483 - 2489. [Abstract] [PDF]
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E. Hay, J. Lemonnier, O. Fromigue, and P. J. Marie Bone Morphogenetic Protein-2 Promotes Osteoblast Apoptosis through a Smad-independent, Protein Kinase C-dependent Signaling Pathway J. Biol. Chem., July 27, 2001; 276(31): 29028 - 29036. [Abstract] [Full Text] [PDF]
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