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The FASEB Journal, Vol 9, 1277-1287, Copyright © 1995 by The Federation of American Societies for Experimental Biology

REVIEWS

The biochemistry of programmed cell death

G Kroemer, P Petit, N Zamzami, JL Vayssiere and B Mignotte
CNRS-UPR420, F-94801 Villejuif, France.

Programmed cell death (PCD) is involved in the removal of superfluous and damaged cells in most organ systems. The induction phase of PCD or apoptosis is characterized by an extreme heterogeneity of potential PCD- triggering signal transduction pathways. During the subsequent effector phase, the numerous PCD-inducing stimuli converge into a few stereotypical pathways and cells pass a point of no return, thus becoming irreversibly committed to death. It is only during the successive degradation phase that vital structures and functions are destroyed, giving rise to the full-blown phenotype of PCD. Evidence is accumulating that cytoplasmic structures, including mitochondria, participate in the critical effector stage and that alterations commonly considered to define PCD (apoptotic morphology of the nucleus and regular, oligonucleosomal chromatin fragmentation) have to be ascribed to the late degradation phase. The decision as to whether a cell will undergo PCD or not may be expected to be regulated by "switches" that, once activated, trigger self-amplificatory metabolic pathways. One of these switches may reside in a perturbation of mitochondrial function. Thus, a decrease in mitochondrial transmembrane potential, followed by mitochondrial uncoupling and generation of reactive oxygen species, precedes nuclear alterations. It appears that molecules that participate in apoptotic decision-making also exert functions that are vital for normal cell proliferation and intermediate metabolism.


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Home page
 Cancer Res.Home page
A. Ushmorov, V. Hack, and W. Droge
Differential Reconstitution of Mitochondrial Respiratory Chain Activity and Plasma Redox State by Cysteine and Ornithine in a Model of Cancer Cachexia
Cancer Res., July 1, 1999; 59(14): 3527 - 3534.
[Abstract] [Full Text] [PDF]

Home page
 CarcinogenesisHome page
J. W. Crott and M. Fenech
Effect of vitamin C supplementation on chromosome damage, apoptosis and necrosis ex vivo
Carcinogenesis, June 1, 1999; 20(6): 1035 - 1041.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
J. M. ESTEVE, J. MOMPO, J. GARCIA DE LA ASUNCION, J. SASTRE, M. ASENSI, J. BOIX, J. R. VIÑA, J. VIÑA, and F. V. PALLARDÓ
Oxidative damage to mitochondrial DNA and glutathione oxidation in apoptosis: studies in vivo and in vitro
FASEB J, June 1, 1999; 13(9): 1055 - 1064.
[Abstract] [Full Text]

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 J. Immunol.Home page
B. Dallaporta, P. Marchetti, M. A. de Pablo, C. Maisse, H.-T. Duc, D. Metivier, N. Zamzami, M. Geuskens, and G. Kroemer
Plasma Membrane Potential in Thymocyte Apoptosis
J. Immunol., June 1, 1999; 162(11): 6534 - 6542.
[Abstract] [Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
G. Kroemer and H. de The
Arsenic Trioxide, a Novel Mitochondriotoxic Anticancer Agent?
J Natl Cancer Inst, May 5, 1999; 91(9): 743 - 745.
[Full Text] [PDF]

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 J. Nutr.Home page
D. Li, J. A. Yee, M. H. McGuire, P. A. Murphy, and L. Yan
Soybean Isoflavones Reduce Experimental Metastasis in Mice
J. Nutr., May 1, 1999; 129(5): 1075 - 1078.
[Abstract] [Full Text]

Home page
 Infect. Immun.Home page
B. Leblebicioglu and J. Walters
Alkaline Conditions Accelerate Polymorphonuclear Leukocyte Apoptosis In Vitro
Infect. Immun., April 1, 1999; 67(4): 2019 - 2021.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
S. Mihara, N. Suzuki, S. Wakisaka, S. Suzuki, N. Sekita, S. Yamamoto, N. Saito, T. Hoshino, and T. Sakane
Effects of Thyroid Hormones on Apoptotic Cell Death of Human Lymphocytes
J. Clin. Endocrinol. Metab., April 1, 1999; 84(4): 1378 - 1385.
[Abstract] [Full Text]

Home page
 Am. J. Physiol. Renal Physiol.Home page
Y.-L. Guo, B. Kang, L.-J. Yang, and J. R. Williamson
Tumor necrosis factor-alpha and ceramide induce cell death through different mechanisms in rat mesangial cells
Am J Physiol Renal Physiol, March 1, 1999; 276(3): F390 - F397.
[Abstract] [Full Text] [PDF]

Home page
 BloodHome page
J. Dimitroulakos, D. Nohynek, K. L. Backway, D. W. Hedley, H. Yeger, M. H. Freedman, M. D. Minden, and L. Z. Penn
Increased Sensitivity of Acute Myeloid Leukemias to Lovastatin-Induced Apoptosis: A Potential Therapeutic Approach
Blood, February 15, 1999; 93(4): 1308 - 1318.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
W. Yu, K. Israel, Q. Y. Liao, C. M. Aldaz, B. G. Sanders, and K. Kline
Vitamin E Succinate (VES) Induces Fas Sensitivity in Human Breast Cancer Cells: Role for Mr 43,000 Fas in VES-triggered Apoptosis
Cancer Res., February 1, 1999; 59(4): 953 - 961.
[Abstract] [Full Text] [PDF]

Home page
 JEMHome page
S. A. Susin, H. K. Lorenzo, N. Zamzami, I. Marzo, C. Brenner, N. Larochette, M.-C. Prevost, P. M. Alzari, and G. Kroemer
Mitochondrial Release of Caspase-2 and -9 during the Apoptotic Process
J. Exp. Med., January 18, 1999; 189(2): 381 - 394.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
J. J. Lemasters
V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis
Am J Physiol Gastrointest Liver Physiol, January 1, 1999; 276(1): G1 - G6.
[Abstract] [Full Text] [PDF]

Home page
 FASEB J.Home page
U. Rauen, B. Polzar, H. Stephan, H. G. Mannherz, and H. D. Groot
Cold-induced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species
FASEB J, January 1, 1999; 13(1): 155 - 168.
[Abstract] [Full Text]

Home page
 J. Biol. Chem.Home page
D. D. Bannerman, M. Sathyamoorthy, and S. E. Goldblum
Bacterial Lipopolysaccharide Disrupts Endothelial Monolayer Integrity and Survival Signaling Events through Caspase Cleavage of Adherens Junction Proteins
J. Biol. Chem., December 25, 1998; 273(52): 35371 - 35380.
[Abstract] [Full Text] [PDF]

Home page
 FASEB J.Home page
G. Lizard, S. Gueldry, O. Sordet, S. Monier, A. Athias, C. Miguet, G. Bessede, S. Lemaire, E. Solary, and P. Gambert
Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production
FASEB J, December 1, 1998; 12(15): 1651 - 1663.
[Abstract] [Full Text]

Home page
 Am. J. Pathol.Home page
H. W. Sohn, E. Y. Choi, S. H. Kim, I.-s. Lee, D. H. Chung, U. A Sung, D. H. Hwang, S. S. Cho, B. H. Jun, J. J. Jang, et al.
Engagement of CD99 Induces Apoptosis Through a Calcineurin-Independent Pathway in Ewing's Sarcoma Cells
Am. J. Pathol., December 1, 1998; 153(6): 1937 - 1945.
[Abstract] [Full Text] [PDF]

Home page
 J. Histochem. Cytochem.Home page
S. Angermüller, G. Künstle, and G. Tiegs
Pre-apoptotic Alterations in Hepatocytes of TNF{alpha}-treated Galactosamine-sensitized Mice
J. Histochem. Cytochem., October 1, 1998; 46(10): 1175 - 1184.
[Abstract] [Full Text]

Home page
 Am. J. Respir. Cell Mol. Bio.Home page
H. Jyonouchi, S. Sun, T. Abiru, S. Chareancholvanich, and D. H. Ingbar
The Effects of Hyperoxic Injury and Antioxidant Vitamins on Death and Proliferation of Human Small Airway Epithelial Cells
Am. J. Respir. Cell Mol. Biol., September 1, 1998; 19(3): 426 - 436.
[Abstract] [Full Text]

Home page
 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
S. Rounds, W. L. Yee, D. D. Dawicki, E. Harrington, N. Parks, and M. V. Cutaia
Mechanism of extracellular ATP- and adenosine-induced apoptosis of cultured pulmonary artery endothelial cells
Am J Physiol Lung Cell Mol Physiol, August 1, 1998; 275(2): L379 - L388.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
N. A. Al-Abdulla and L. J. Martin
Apoptosis of Retrogradely Degenerating Neurons Occurs in Association with the Accumulation of Perikaryal Mitochondria and Oxidative Damage to the Nucleus
Am. J. Pathol., August 1, 1998; 153(2): 447 - 456.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
H. He, P. A. Hershberger, and S. A. McCarthy
Characterization of a Novel Bax-Associated Protein Expressed in Hemopoietic Tissues and Regulated During Thymocyte Apoptosis
J. Immunol., August 1, 1998; 161(3): 1169 - 1175.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
A.-K. Yi, M. Chang, D. W. Peckham, A. M. Krieg, and R. F. Ashman
CpG Oligodeoxyribonucleotides Rescue Mature Spleen B Cells from Spontaneous Apoptosis and Promote Cell Cycle Entry
J. Immunol., June 15, 1998; 160(12): 5898 - 5906.
[Abstract] [Full Text] [PDF]

Home page
 Infect. Immun.Home page
C. Fiorentini, A. Fabbri, L. Falzano, A. Fattorossi, P. Matarrese, R. Rivabene, and G. Donelli
Clostridium difficile Toxin B Induces Apoptosis in Intestinal Cultured Cells
Infect. Immun., June 1, 1998; 66(6): 2660 - 2665.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
B. Dallaporta, T. Hirsch, S. A. Susin, N. Zamzami, N. Larochette, C. Brenner, I. Marzo, and G. Kroemer
Potassium Leakage During the Apoptotic Degradation Phase
J. Immunol., June 1, 1998; 160(11): 5605 - 5615.
[Abstract] [Full Text] [PDF]

Home page
 JEMHome page
D. Vercammen, R. Beyaert, G. Denecker, V. Goossens, G. Van Loo, W. Declercq, J. Grooten, W. Fiers, and P. Vandenabeele
Inhibition of Caspases Increases the Sensitivity of L929 Cells to Necrosis Mediated by Tumor Necrosis Factor
J. Exp. Med., May 4, 1998; 187(9): 1477 - 1485.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
M. K. A. Bauer, M. Vogt, M. Los, J. Siegel, S. Wesselborg, and K. Schulze-Osthoff
Role of Reactive Oxygen Intermediates in Activation-induced CD95 (APO-1/Fas) Ligand Expression
J. Biol. Chem., April 3, 1998; 273(14): 8048 - 8055.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
I Farkas, L Baranyi, M Takahashi, A Fukuda, Z. Liposits, T Yamamoto, and H Okada
A neuronal C5a receptor and an associated apoptotic signal transduction pathway
J. Physiol., March 15, 1998; 507(3): 679 - 687.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Pharmacol.Home page
L. Ramamoorthy and I. R. Tizard
Induction of Apoptosis in a Macrophage Cell Line RAW 264.7 By Acemannan, a beta -(1,4)-Acetylated Mannan
Mol. Pharmacol., March 1, 1998; 53(3): 415 - 421.
[Abstract] [Full Text]

Home page
 Cardiovasc ResHome page
R. Ferrari
Tumor necrosis factor in CHF: a double facet cytokine
Cardiovasc Res, March 1, 1998; 37(3): 554 - 559.
[Full Text] [PDF]

Home page
 JEMHome page
H. Hirata, A. Takahashi, S. Kobayashi, S. Yonehara, H. Sawai, T. Okazaki, K. Yamamoto, and M. Sasada
Caspases Are Activated in a Branched Protease Cascade and Control Distinct Downstream Processes in Fas-induced Apoptosis
J. Exp. Med., February 16, 1998; 187(4): 587 - 600.
[Abstract] [Full Text] [PDF]

Home page
 JCBHome page
J. N. Lavoie, M. Nguyen, R.C. Marcellus, P.E. Branton, and G.C. Shore
E4orf4, a Novel Adenovirus Death Factor That Induces p53-independent Apoptosis by a Pathway That Is Not Inhibited by zVAD-fmk
J. Cell Biol., February 9, 1998; 140(3): 637 - 645.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
T. Noda, R. Iwakiri, K. Fujimoto, S. Matsuo, and T. Y. Aw
Programmed cell death induced by ischemia-reperfusion in rat intestinal mucosa
Am J Physiol Gastrointest Liver Physiol, February 1, 1998; 274(2): G270 - G276.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
Z. Wang and D. M. Templeton
Induction of c-fos Proto-oncogene in Mesangial Cells by Cadmium
J. Biol. Chem., January 2, 1998; 273(1): 73 - 79.
[Abstract] [Full Text] [PDF]


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