This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gorczyca, W. Articles by Darzynkiewicz, Z. Search for Related Content PubMed PubMed Citation Articles by Gorczyca, W. Articles by Darzynkiewicz, Z.

Detection of DNA Strand Breaks in Individual Apoptotic Cells by the in Situ Terminal Deoxynucleotidyl Transferase and Nick Translation Assays¹

The Cancer Research Institute, New York Medical College, Valhalla, New York, 10595

DNA strand breaks which occur in HL-60 cells as a result of activation of endonuclease during apoptosis induced by cell treatment with the DNA topoisomerase I inhibitor camptothecin and topoisomerase II inhibitors teniposide, 4'-(9-acridinylamino)-3-methanesulfon-m-anisidide, and fostriecin were labeled in situ, in individual fixed and permeabilized cells, with biotinylated dUTP (detected by fluoresceinated avidin), using the terminal deoxynucleotidyl transferase or nick translation assays. During the early stage of apoptosis, prior to nuclear fragmentation, the breaks were predominantly localized at the nuclear periphery, close to the nuclear envelope. In more advanced stages, all cellular DNA, then localized within the cell as dense, homogeneous granules of a variety of sizes, was strongly labeled, indicating extensive and more uniform distribution of breaks throughout genomic DNA. Bivariate analysis of the incorporated biotinylated dUTP and cellular DNA content by flow cytometry made it possible to estimate the kinetics of the labeling reaction and relate DNA breaks to cell position in the cycle. The kinetics of biotinylated dUTP incorporation was faster, and the distinction of cells with DNA breaks was more pronounced, using the terminal transferase rather than the nick translation assay. Camptothecin, teniposide, and 4'-(9-acridinylamino)-3-methanesulfon-m-anisidide induced DNA breaks preferentially in S-phase cells, having little effect on cells in the G₁ phase of the cycle. In contrast, fostriecin affected cells indiscriminately, in all phases of the cell cycle. The method of detection of DNA strand breaks (3'-hydroxyl termini) individual cells offers several advantages and can be applied to clinical material (tumor biopsies) to study the induction of apoptosis in tumors during treatment, as a possible prognostic marker. The protein-associated DNA breaks in the "cleavable" DNA-topoisoerase complexes, which are the primary lesions induced by the inhibitors and precede apoptosis, were not detectable by the present methods.

¹ Supported by USPHS Grant RO1 CA28704 and the Carl Inserra Fund. J. G. is a recipient of the fellowship established by the "This Close" Foundation for Cancer Research.

² To whom requests for reprints should be addressed, at the Cancer Research Institute, New York Medical College, 100 Grasslands Road, Elmsford, NY 10523.

Received 10/ 9/92. Accepted 2/ 4/93.

This article has been cited by other articles:

				S. Wu, Y.-C. Hu, H. Liu, and Y. Shi Loss of YY1 Impacts the Heterochromatic State and Meiotic Double-Strand Breaks during Mouse Spermatogenesis Mol. Cell. Biol., December 1, 2009; 29(23): 6245 - 6256. [Abstract] [Full Text] [PDF]

				H. P. Dong, A. Holth, L. Kleinberg, M. G. Ruud, M. B. Elstrand, C. G. Trope, B. Davidson, and B. Risberg Evaluation of Cell Surface Expression of Phosphatidylserine in Ovarian Carcinoma Effusions Using the Annexin-V/7-AAD Assay: Clinical Relevance and Comparison With Other Apoptosis Parameters Am J Clin Pathol, November 1, 2009; 132(5): 756 - 762. [Abstract] [Full Text] [PDF]

				K. D. Belanger, D. Walter, T. A. Henderson, A. L. Yelton, T. G. O'Brien, K. G. Belanger, S. J. Geier, and B. Fahrenkrog Nuclear localisation is crucial for the proapoptotic activity of the HtrA-like serine protease Nma111p J. Cell Sci., November 1, 2009; 122(21): 3931 - 3941. [Abstract] [Full Text] [PDF]

				W. BECHTEL and G. BAUER Catalase Protects Tumor Cells from Apoptosis Induction by Intercellular ROS Signaling Anticancer Res, November 1, 2009; 29(11): 4541 - 4557. [Abstract] [Full Text] [PDF]

				K.-S. Choi, E.-K. Song, and C.-Y. Yim Cytokines secreted by IL-2-activated lymphocytes induce endogenous nitric oxide synthesis and apoptosis in macrophages J. Leukoc. Biol., June 1, 2008; 83(6): 1440 - 1450. [Abstract] [Full Text] [PDF]

				S. E. M. Lewis and I. M. Agbaje Using the alkaline comet assay in prognostic tests for male infertility and assisted reproductive technology outcomes Mutagenesis, May 1, 2008; 23(3): 163 - 170. [Abstract] [Full Text] [PDF]

				R. Kondo, K. V. Gleixner, M. Mayerhofer, A. Vales, A. Gruze, P. Samorapoompichit, K. Greish, M.-T. Krauth, K. J. Aichberger, W. F. Pickl, et al. Identification of heat shock protein 32 (Hsp32) as a novel survival factor and therapeutic target in neoplastic mast cells Blood, July 15, 2007; 110(2): 661 - 669. [Abstract] [Full Text] [PDF]

				J. L. Rose, K. C. Reeves, R. I. Likhotvorik, and D. G. Hoyt Base Excision Repair Proteins Are Required for Integrin-Mediated Suppression of Bleomycin-Induced DNA Breakage in Murine Lung Endothelial Cells J. Pharmacol. Exp. Ther., April 1, 2007; 321(1): 318 - 326. [Abstract] [Full Text] [PDF]

				M. Long, A. Stronati, D. Bizzaro, T. Kruger, G.-C. Manicardi, P. S Hjelmborg, M. Spano, A. Giwercman, G. Toft, J. P. Bonde, et al. Relation between serum xenobiotic-induced receptor activities and sperm DNA damage and sperm apoptotic markers in European and Inuit populations Reproduction, February 1, 2007; 133(2): 517 - 530. [Abstract] [Full Text] [PDF]

				A Stronati, G C Manicardi, M Cecati, M Bordicchia, L Ferrante, M Spano, G Toft, J P Bonde, B A G Jonsson, A Rignell-Hydbom, et al. Relationships between sperm DNA fragmentation, sperm apoptotic markers and serum levels of CB-153 and p,p'-DDE in European and Inuit populations. Reproduction, December 1, 2006; 132(6): 949 - 958. [Abstract] [Full Text] [PDF]

				S. Ying, S. F. Fischer, M. Pettengill, D. Conte, S. A. Paschen, D. M. Ojcius, and G. Hacker Characterization of Host Cell Death Induced by Chlamydia trachomatis Infect. Immun., November 1, 2006; 74(11): 6057 - 6066. [Abstract] [Full Text] [PDF]

				A. Borini, N. Tarozzi, D. Bizzaro, M.A. Bonu, L. Fava, C. Flamigni, and G. Coticchio Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART Hum. Reprod., November 1, 2006; 21(11): 2876 - 2881. [Abstract] [Full Text] [PDF]

				D. Walter, S. Wissing, F. Madeo, and B. Fahrenkrog The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2 J. Cell Sci., May 1, 2006; 119(9): 1843 - 1851. [Abstract] [Full Text] [PDF]

				A. N. Fatehi, M. M. Bevers, E. Schoevers, B. A. J. Roelen, B. Colenbrander, and B. M. Gadella DNA Damage in Bovine Sperm Does Not Block Fertilization and Early Embryonic Development But Induces Apoptosis After the First Cleavages J Androl, March 1, 2006; 27(2): 176 - 188. [Abstract] [Full Text] [PDF]

				T. Said, A. Agarwal, S. Grunewald, M. Rasch, T. Baumann, C. Kriegel, L. Li, H.-J. Glander, A. J. Thomas Jr., and U. Paasch Selection of Nonapoptotic Spermatozoa As a New Tool for Enhancing Assisted Reproduction Outcomes: An In Vitro Model Biol Reprod, March 1, 2006; 74(3): 530 - 537. [Abstract] [Full Text] [PDF]

				K. V. Gleixner, M. Mayerhofer, K. J. Aichberger, S. Derdak, K. Sonneck, A. Bohm, A. Gruze, P. Samorapoompichit, P. W. Manley, D. Fabbro, et al. PKC412 inhibits in vitro growth of neoplastic human mast cells expressing the D816V-mutated variant of KIT: comparison with AMN107, imatinib, and cladribine (2CdA) and evaluation of cooperative drug effects Blood, January 15, 2006; 107(2): 752 - 759. [Abstract] [Full Text] [PDF]

				N. Berkova, S. Lair-Fulleringer, F. Femenia, D. Huet, M.-C. Wagner, K. Gorna, F. Tournier, O. Ibrahim-Granet, J. Guillot, R. Chermette, et al. Aspergillus fumigatus conidia inhibit tumour necrosis factor- or staurosporine-induced apoptosis in epithelial cells Int. Immunol., January 1, 2006; 18(1): 139 - 150. [Abstract] [Full Text] [PDF]

				Q. Luo, Y. Ding, K. Watson, J. Zhang, and G.-H. Fan N-Methyl-D-aspartate Attenuates CXCR2-Mediated Neuroprotection through Enhancing the Receptor Phosphorylation and Blocking the Receptor Recycling Mol. Pharmacol., August 1, 2005; 68(2): 528 - 537. [Abstract] [Full Text] [PDF]

				A. Barak, T. Goldkorn, and L. S. Morse Laser Induces Apoptosis and Ceramide Production in Human Retinal Pigment Epithelial Cells Invest. Ophthalmol. Vis. Sci., July 1, 2005; 46(7): 2587 - 2591. [Abstract] [Full Text] [PDF]

				F. A.T. de Vries, E. de Boer, M. van den Bosch, W. M. Baarends, M. Ooms, L. Yuan, J.-G. Liu, A. A. van Zeeland, C. Heyting, and A. Pastink Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation Genes & Dev., June 1, 2005; 19(11): 1376 - 1389. [Abstract] [Full Text] [PDF]

				T. Dong, G. Stewart-Jones, N. Chen, P. Easterbrook, X. Xu, L. Papagno, V. Appay, M. Weekes, C. Conlon, C. Spina, et al. HIV-specific Cytotoxic T Cells from Long-Term Survivors Select a Unique T Cell Receptor J. Exp. Med., December 20, 2004; 200(12): 1547 - 1557. [Abstract] [Full Text] [PDF]

				D. Diaz, A. Prieto, H. Barcenilla, J. Monserrat, P. Prieto, M. A. Sanchez, E. Reyes, M. P. Hernandez-Fuentes, A. de la Hera, A. Orfao, et al. Loss of lineage antigens is a common feature of apoptotic lymphocytes J. Leukoc. Biol., September 1, 2004; 76(3): 609 - 615. [Abstract] [Full Text] [PDF]

				E. Tourkina, P. Gooz, J. C. Oates, A. Ludwicka-Bradley, R. M. Silver, and S. Hoffman Curcumin-Induced Apoptosis in Scleroderma Lung Fibroblasts: Role of Protein Kinase C{epsilon} Am. J. Respir. Cell Mol. Biol., July 1, 2004; 31(1): 28 - 35. [Abstract] [Full Text] [PDF]

				D. Paisley, S. Banks, J. Selfridge, N. F. McLennan, A.-M. Ritchie, C. McEwan, D. S. Irvine, P. T. K. Saunders, J. C. Manson, and D. W. Melton Male Infertility and DNA Damage in Doppel Knockout and Prion Protein/Doppel Double-Knockout Mice Am. J. Pathol., June 1, 2004; 164(6): 2279 - 2288. [Abstract] [Full Text] [PDF]

				A. Solhaug, M. Refsnes, M. Lag, P. E. Schwarze, T. Husoy, and J. A. Holme Polycyclic aromatic hydrocarbons induce both apoptotic and anti-apoptotic signals in Hepa1c1c7 cells Carcinogenesis, May 1, 2004; 25(5): 809 - 819. [Abstract] [Full Text] [PDF]

				A. Gilhar, Y. Ullmann, R. Karry, R. Shalaginov, B. Assy, S. Serafimovich, and R. S. Kalish Aging of Human Epidermis: Reversal of Aging Changes Correlates With Reversal of Keratinocyte Fas Expression and Apoptosis J Gerontol A Biol Sci Med Sci, May 1, 2004; 59(5): B411 - B415. [Abstract] [Full Text] [PDF]

				S. Lotz, E. Aga, I. Wilde, G. van Zandbergen, T. Hartung, W. Solbach, and T. Laskay Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2 J. Leukoc. Biol., March 1, 2004; 75(3): 467 - 477. [Abstract] [Full Text] [PDF]

				S. Pacini, M. Pellegrini, E. Migliaccio, L. Patrussi, C. Ulivieri, A. Ventura, F. Carraro, A. Naldini, L. Lanfrancone, P. Pelicci, et al. p66SHC Promotes Apoptosis and Antagonizes Mitogenic Signaling in T Cells Mol. Cell. Biol., February 15, 2004; 24(4): 1747 - 1757. [Abstract] [Full Text] [PDF]

				G. van Zandbergen, J. Gieffers, H. Kothe, J. Rupp, A. Bollinger, E. Aga, M. Klinger, H. Brade, K. Dalhoff, M. Maass, et al. Chlamydia pneumoniae Multiply in Neutrophil Granulocytes and Delay Their Spontaneous Apoptosis J. Immunol., February 1, 2004; 172(3): 1768 - 1776. [Abstract] [Full Text] [PDF]

				L. Gabriele, P. Borghi, C. Rozera, P. Sestili, M. Andreotti, A. Guarini, E. Montefusco, R. Foa, and F. Belardelli IFN-{alpha} promotes the rapid differentiation of monocytes from patients with chronic myeloid leukemia into activated dendritic cells tuned to undergo full maturation after LPS treatment Blood, February 1, 2004; 103(3): 980 - 987. [Abstract] [Full Text] [PDF]

				B. Fahrenkrog, U. Sauder, and U. Aebi The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis J. Cell Sci., January 1, 2004; 117(1): 115 - 126. [Abstract] [Full Text] [PDF]

				S. S. Castillo and D. Teegarden Sphingosine-1-Phosphate Inhibition of Apoptosis Requires Mitogen-Activated Protein Kinase Phosphatase-1 in Mouse Fibroblast C3H10T1/2 Cells J. Nutr., November 1, 2003; 133(11): 3343 - 3349. [Abstract] [Full Text] [PDF]

				C. Prehaud, S. Lay, B. Dietzschold, and M. Lafon Glycoprotein of Nonpathogenic Rabies Viruses Is a Key Determinant of Human Cell Apoptosis J. Virol., October 1, 2003; 77(19): 10537 - 10547. [Abstract] [Full Text] [PDF]

				L. I. Rutitzky, G. A. Mirkin, and M. J. Stadecker Apoptosis by Neglect of CD4+ Th Cells in Granulomas: A Novel Effector Mechanism Involved in the Control of Egg-Induced Immunopathology in Murine Schistosomiasis J. Immunol., August 15, 2003; 171(4): 1859 - 1867. [Abstract] [Full Text] [PDF]

				D. R. Beisner, I. H. Chu, A. F. Arechiga, S. M. Hedrick, and C. M. Walsh The Requirements for Fas-Associated Death Domain Signaling in Mature T Cell Activation and Survival J. Immunol., July 1, 2003; 171(1): 247 - 256. [Abstract] [Full Text] [PDF]

				P.-r. Cao, M. M. McHugh, T. Melendy, and T. Beerman The DNA Minor Groove-alkylating Cyclopropylpyrroloindole Drugs Adozelesin and Bizelesin Induce Different DNA Damage Response Pathways in Human Colon Carcinoma HCT116 Cells Mol. Cancer Ther., July 1, 2003; 2(7): 651 - 659. [Abstract] [Full Text] [PDF]

				D. M. Eklund and J. Edqvist Localization of Nonspecific Lipid Transfer Proteins Correlate with Programmed Cell Death Responses during Endosperm Degradation in Euphorbia lagascae Seedlings Plant Physiology, July 1, 2003; 132(3): 1249 - 1259. [Abstract] [Full Text] [PDF]

				W. M. Baarends, E. Wassenaar, J. W. Hoogerbrugge, G. van Cappellen, H. P. Roest, J. Vreeburg, M. Ooms, J. H. J. Hoeijmakers, and J. A. Grootegoed Loss of HR6B Ubiquitin-Conjugating Activity Results in Damaged Synaptonemal Complex Structure and Increased Crossing-Over Frequency during the Male Meiotic Prophase Mol. Cell. Biol., February 15, 2003; 23(4): 1151 - 1162. [Abstract] [Full Text] [PDF]

				R. Hassan, M. R. Lerner, D. Benbrook, S. A. Lightfoot, D. J. Brackett, Q.-C. Wang, and I. Pastan Antitumor Activity of SS(dsFv)PE38 and SS1(dsFv)PE38, Recombinant Antimesothelin Immunotoxins against Human Gynecologic Cancers Grown in Organotypic Culture in Vitro Clin. Cancer Res., November 1, 2002; 8(11): 3520 - 3526. [Abstract] [Full Text] [PDF]

				Y. Dai, T. H. Landowski, S. T. Rosen, P. Dent, and S. Grant Combined treatment with the checkpoint abrogator UCN-01 and MEK1/2 inhibitors potently induces apoptosis in drug-sensitive and -resistant myeloma cells through an IL-6-independent mechanism Blood, October 16, 2002; 100(9): 3333 - 3343. [Abstract] [Full Text] [PDF]

				S. Heigold and G. Bauer RAW 264.7 macrophages induce apoptosis selectively in transformed fibroblasts: intercellular signaling based on reactive oxygen and nitrogen species J. Leukoc. Biol., September 1, 2002; 72(3): 554 - 563. [Abstract] [Full Text] [PDF]

				C. GIULIANI, G. CONSONNI, G. GAVAZZI, M. COLOMBO, and S. DOLFINI Programmed Cell Death during Embryogenesis in Maize Ann. Bot., August 1, 2002; 90(2): 287 - 292. [Abstract] [Full Text] [PDF]

				E. Aga, D. M. Katschinski, G. van Zandbergen, H. Laufs, B. Hansen, K. Muller, W. Solbach, and T. Laskay Inhibition of the Spontaneous Apoptosis of Neutrophil Granulocytes by the Intracellular Parasite Leishmania major J. Immunol., July 15, 2002; 169(2): 898 - 905. [Abstract] [Full Text] [PDF]

				B.M. Gadella and R.A.P. Harrison Capacitation Induces Cyclic Adenosine 3',5'-Monophosphate-Dependent, but Apoptosis-Unrelated, Exposure of Aminophospholipids at the Apical Head Plasma Membrane of Boar Sperm Cells Biol Reprod, July 1, 2002; 67(1): 340 - 350. [Abstract] [Full Text] [PDF]

				S. Heigold, C. Sers, W. Bechtel, B. Ivanovas, R. Schafer, and G. Bauer Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts Carcinogenesis, June 1, 2002; 23(6): 929 - 941. [Abstract] [Full Text] [PDF]

				E. Hellsten, D. J. Bernard, J. W. Owens, M. Eckhaus, S. F. Suchy, and R. L. Nussbaum Sertoli Cell Vacuolization and Abnormal Germ Cell Adhesion in Mice Deficient in an Inositol Polyphosphate 5-Phosphatase Biol Reprod, May 1, 2002; 66(5): 1522 - 1530. [Abstract] [Full Text]

				S.-B. Ning, L. Wang, and Y.-C. Song Identification of programmed cell death in situ in individual plant cells in vivo using a chromosome preparation technique J. Exp. Bot., April 1, 2002; 53(369): 651 - 658. [Abstract] [Full Text] [PDF]

				T. Hawighorst, M. Skobe, M. Streit, Y.-K. Hong, P. Velasco, L. F. Brown, L. Riccardi, B. Lange-Asschenfeldt, and M. Detmar Activation of the Tie2 Receptor by Angiopoietin-1 Enhances Tumor Vessel Maturation and Impairs Squamous Cell Carcinoma Growth Am. J. Pathol., April 1, 2002; 160(4): 1381 - 1392. [Abstract] [Full Text] [PDF]

				M Jarvis, U Schulz, A M Dickinson, L Sviland, G Jackson, A Konur, X N Wang, I Hromadnikova, H J Kolb, G Eissner, et al. The detection of apoptosis in a human in vitro skin explant assay for graft versus host reactions J. Clin. Pathol., February 1, 2002; 55(2): 127 - 132. [Abstract] [Full Text] [PDF]

				Y. Tong, Q. Yang, C. Vater, L.K. Venkatesh, D. Custeau, T. Chittenden, G. Chinnadurai, and H. Gourdeau The Pro-apoptotic Protein, Bik, Exhibits Potent Antitumor Activity That Is Dependent on Its BH3 Domain Mol. Cancer Ther., December 1, 2001; 1(2): 95 - 102. [Abstract] [Full Text] [PDF]

				N. Richards, P. Schaner, A. Diaz, J. Stuckey, E. Shelden, A. Wadhwa, and D. L. Gumucio Interaction between Pyrin and the Apoptotic Speck Protein (ASC) Modulates ASC-induced Apoptosis J. Biol. Chem., October 12, 2001; 276(42): 39320 - 39329. [Abstract] [Full Text] [PDF]

				A. Schwieger, L. Bauer, J. Hanusch, C. Sers, R. Schafer, and G. Bauer ras oncogene expression determines sensitivity for intercellular induction of apoptosis Carcinogenesis, September 1, 2001; 22(9): 1385 - 1392. [Abstract] [Full Text] [PDF]

				M. Volante, M. Papotti, P. Gugliotta, A. Migheli, and G. Bussolati Extensive DNA Fragmentation in Oxyphilic Cell Lesions of the Thyroid J. Histochem. Cytochem., August 1, 2001; 49(8): 1003 - 1012. [Abstract] [Full Text] [PDF]

				Y. Dai, C. Yu, V. Singh, L. Tang, Z. Wang, R. McInistry, P. Dent, and S. Grant Pharmacological Inhibitors of the Mitogen-activated Protein Kinase (MAPK) Kinase/MAPK Cascade Interact Synergistically with UCN-01 to Induce Mitochondrial Dysfunction and Apoptosis in Human Leukemia Cells Cancer Res., July 1, 2001; 61(13): 5106 - 5115. [Abstract] [Full Text] [PDF]

				G. Mehes, A. Witt, E. Kubista, and P. F. Ambros Circulating Breast Cancer Cells Are Frequently Apoptotic Am. J. Pathol., July 1, 2001; 159(1): 17 - 20. [Abstract] [Full Text] [PDF]

				E. V. Thrane, M. Refsnes, G. H. Thoresen, M. Lag, and P. E. Schwarze Fluoride-Induced Apoptosis in Epithelial Lung Cells Involves Activation of MAP Kinases p38 and Possibly JNK Toxicol. Sci., May 1, 2001; 61(1): 83 - 91. [Abstract] [Full Text] [PDF]

				C. Ramos, M. Montano, J. Garcia-Alvarez, V. Ruiz, B. D. Uhal, M. Selman, and A. Pardo Fibroblasts from Idiopathic Pulmonary Fibrosis and Normal Lungs Differ in Growth Rate, Apoptosis, and Tissue Inhibitor of Metalloproteinases Expression Am. J. Respir. Cell Mol. Biol., May 1, 2001; 24(5): 591 - 598. [Abstract] [Full Text]

				K. L. Serrao, J. D. Fortenberry, M. L. Owens, F. L. Harris, and L. A. S. Brown Neutrophils induce apoptosis of lung epithelial cells via release of soluble Fas ligand Am J Physiol Lung Cell Mol Physiol, February 1, 2001; 280(2): L298 - L305. [Abstract] [Full Text] [PDF]

				T. Yamada, W. Marubashi, and M. Niwa Facile Induction of Apoptosis into Plant Cells Associated with Temperature-Sensitive Lethality Shown on Interspecific Hybrid from the Cross Nicotiana suaveolens N. tabacum Plant Cell Physiol., February 1, 2001; 42(2): 204 - 213. [Abstract] [Full Text] [PDF]

				A. Barak, L. S. Morse, and T. Goldkorn Ceramide: A Potential Mediator of Apoptosis in Human Retinal Pigment Epithelial Cells Invest. Ophthalmol. Vis. Sci., January 1, 2001; 42(1): 247 - 254. [Abstract] [Full Text]

				C. B. Jones, J. McIntosh, H. Huang, A. Graytock, and D. G. Hoyt Regulation of Bleomycin-Induced DNA Breakage and Chromatin Structure in Lung Endothelial Cells by Integrins and Poly(ADP-Ribose) Polymerase Mol. Pharmacol., January 1, 2001; 59(1): 69 - 75. [Abstract] [Full Text]

				K. Matsunaga, H. Iijima, and H. Kobayashi Neonatal Inoculation with the Protein-bound Polysaccharide PSK Increases Resistance of Adult Animals to Challenge with Syngeneic Tumor Cells and Reduces Azoxymethane- induced Precancerous Lesions in the Colon Cancer Epidemiol. Biomarkers Prev., December 1, 2000; 9(12): 1313 - 1322. [Abstract] [Full Text]

				B. C. Lewis, J. E. Prescott, S. E. Campbell, H. Shim, R. Z. Orlowski, and C. V. Dang Tumor Induction by the c-Myc Target Genes rcl and Lactate Dehydrogenase A Cancer Res., November 1, 2000; 60(21): 6178 - 6183. [Abstract] [Full Text]

				K. Fettucciari, E. Rosati, L. Scaringi, P. Cornacchione, G. Migliorati, R. Sabatini, I. Fetriconi, R. Rossi, and P. Marconi Group B Streptococcus Induces Apoptosis in Macrophages J. Immunol., October 1, 2000; 165(7): 3923 - 3933. [Abstract] [Full Text] [PDF]

				T. Asai, J. M. Stone, J. E. Heard, Y. Kovtun, P. Yorgey, J. Sheen, and F. M. Ausubel Fumonisin B1-Induced Cell Death in Arabidopsis Protoplasts Requires Jasmonate-, Ethylene-, and Salicylate-Dependent Signaling Pathways PLANT CELL, October 1, 2000; 12(10): 1823 - 1836. [Abstract] [Full Text]

				S. M. Quirk, R. M. Harman, S. C. Huber, and R. G. Cowan Responsiveness of Mouse Corpora Luteal Cells to Fas Antigen (CD95)-Mediated Apoptosis Biol Reprod, July 1, 2000; 63(1): 49 - 56. [Abstract] [Full Text]

				C. A. M. Jamieson and K. R. Yamamoto Crosstalk pathway for inhibition of glucocorticoid-induced apoptosis by T cell receptor signaling PNAS, June 20, 2000; 97(13): 7319 - 7324. [Abstract] [Full Text] [PDF]

				R. P. Kline, E. X. Wu, D. P. Petrylak, M. Szabolcs, P. O. Alderson, M. L. Weisfeldt, P. Cannon, and J. Katz Rapid in Vivo Monitoring of Chemotherapeutic Response Using Weighted Sodium Magnetic Resonance Imaging Clin. Cancer Res., June 1, 2000; 6(6): 2146 - 2156. [Abstract] [Full Text]

				T. Kuwata, I-M. Wang, T. Tamura, R. M. Ponnamperuma, R. Levine, K. L. Holmes, H. C. Morse III, L. M. De Luca, and K. Ozato Vitamin A deficiency in mice causes a systemic expansion of myeloid cells Blood, June 1, 2000; 95(11): 3349 - 3356. [Abstract] [Full Text] [PDF]

				C. Chan and T. Goldkorn Ceramide Path in Human Lung Cell Death Am. J. Respir. Cell Mol. Biol., April 1, 2000; 22(4): 460 - 468. [Abstract] [Full Text]

				K. Takaba, K. Saeki, K. Suzuki, H. Wanibuchi, and S. Fukushima Significant overexpression of metallothionein and cyclin D1 and apoptosis in the early process of rat urinary bladder carcinogenesis induced by treatment with N-butyl-N-(4-hydroxybutyl)nitrosamine or sodium L-ascorbate Carcinogenesis, April 1, 2000; 21(4): 691 - 700. [Abstract] [Full Text] [PDF]

				M. Jenkins, M. Keir, and J. M. McCune A Membrane-bound Fas Decoy Receptor Expressed by Human Thymocytes J. Biol. Chem., March 10, 2000; 275(11): 7988 - 7993. [Abstract] [Full Text] [PDF]

				L. O'Connor, A. W. Harris, and A. Strasser CD95 (Fas/APO-1) and p53 Signal Apoptosis Independently in Diverse Cell Types Cancer Res., March 1, 2000; 60(5): 1217 - 1220. [Abstract] [Full Text]

				J R Paxton, B S Bolger, A Armour, R P Symonds, J H Mao, and R A Burnett Apoptosis in cervical squamous carcinoma: predictive value for survival following radiotherapy J. Clin. Pathol., March 1, 2000; 53(3): 197 - 200. [Abstract] [Full Text] [PDF]

				X. Yang, N. Ma, M. J. Szabolcs, J. Zhong, E. Athan, R. R. Sciacca, R. E. Michler, G. D. Anderson, J. F. Wiese, K. M. Leahy, et al. Upregulation of COX-2 During Cardiac Allograft Rejection Circulation, February 1, 2000; 101(4): 430 - 438. [Abstract] [Full Text] [PDF]

				G Alvarez-Bolado, X Zhou, A. Voss, T Thomas, and P Gruss Winged helix transcription factor Foxb1 is essential for access of mammillothalamic axons to the thalamus Development, January 3, 2000; 127(5): 1029 - 1038. [Abstract] [PDF]

				S. E. Blutt, T. J. McDonnell, T. C. Polek, and N. L. Weigel Calcitriol-Induced Apoptosis in LNCaP Cells Is Blocked By Overexpression of Bcl-2 Endocrinology, January 1, 2000; 141(1): 10 - 17. [Abstract] [Full Text] [PDF]

				F. Turturro, P. Seth, and C. J. Link Jr. In Vitro Adenoviral Vector p53-mediated Transduction and Killing Correlates with Expression of Coxsackie-Adenovirus Receptor and {{alpha}}{{nu}}{beta}5 Integrin in SUDHL-1 Cells Derived from Anaplastic Large-Cell Lymphoma Clin. Cancer Res., January 1, 2000; 6(1): 185 - 192. [Abstract] [Full Text]

				M. Streit, L. Riccardi, P. Velasco, L. F. Brown, T. Hawighorst, P. Bornstein, and M. Detmar Thrombospondin-2: A potent endogenous inhibitor of tumor growth and angiogenesis PNAS, December 21, 1999; 96(26): 14888 - 14893. [Abstract] [Full Text] [PDF]

				Y. X. Schwarz, M.-y. Yang, D. Qin, J. Wu, W. D. Jarvis, S. Grant, G. F. Burton, A. K. Szakal, and J. G. Tew Follicular Dendritic Cells Protect Malignant B Cells from Apoptosis Induced by Anti-Fas and Antineoplastic Agents J. Immunol., December 15, 1999; 163(12): 6442 - 6447. [Abstract] [Full Text] [PDF]

				E. S. Berleth, S. Nadadur, A. D. Henn, C. Eppolito, S. Shiojiri, H. L. Gurtoo, M. J. Ehrke, and E. Mihich Identification, Characterization, and Cloning of TIP-B1, a Novel Protein Inhibitor of Tumor Necrosis Factor-induced Lysis Cancer Res., November 1, 1999; 59(21): 5497 - 5506. [Abstract] [Full Text] [PDF]

				R. Liu, T. Itoh, K.-i. Arai, and S. Watanabe Two Distinct Signaling Pathways Downstream of Janus Kinase 2 Play Redundant Roles for Antiapoptotic Activity of Granulocyte-Macrophage Colony-stimulating Factor Mol. Biol. Cell, November 1, 1999; 10(11): 3959 - 3970. [Abstract] [Full Text]

				V. D. Kravtsov, T. O. Daniel, and M. J. Koury Comparative Analysis of Different Methodological Approaches to the in Vitro Study of Drug-Induced Apoptosis Am. J. Pathol., October 1, 1999; 155(4): 1327 - 1339. [Abstract] [Full Text] [PDF]

				R. D. Glick, S. L. Swendeman, D. C. Coffey, R. A. Rifkind, P. A. Marks, V. M. Richon, and M. P. La Quaglia Hybrid Polar Histone Deacetylase Inhibitor Induces Apoptosis and CD95/CD95 Ligand Expression in Human Neuroblastoma Cancer Res., September 1, 1999; 59(17): 4392 - 4399. [Abstract] [Full Text] [PDF]

				L. Gabriele, J. Phung, J. Fukumoto, D. Segal, I-M. Wang, P. Giannakakou, N. A. Giese, K. Ozato, and H. C. Morse III Regulation of Apoptosis in Myeloid Cells by Interferon Consensus Sequence-Binding Protein J. Exp. Med., August 2, 1999; 190(3): 411 - 422. [Abstract] [Full Text] [PDF]

				Q. Li and C. V. Dang c-Myc Overexpression Uncouples DNA Replication from Mitosis Mol. Cell. Biol., August 1, 1999; 19(8): 5339 - 5351. [Abstract] [Full Text] [PDF]

				R. G. Dullea, J. F. Robinson, and J. S. Bedford Nonrandom Degradation of DNA in Human Leukemic Cells during Radiation-induced Apoptosis Cancer Res., August 1, 1999; 59(15): 3712 - 3718. [Abstract] [Full Text] [PDF]

				M. S. Mendonca, K. L. Howard, D. L. Farrington, L. A. Desmond, T. M. Temples, B. M. Mayhugh, J. J. Pink, and D. A. Boothman Delayed Apoptotic Responses Associated with Radiation-induced Neoplastic Transformation of Human Hybrid Cells Cancer Res., August 1, 1999; 59(16): 3972 - 3979. [Abstract] [Full Text] [PDF]

				M. Streit, P. Velasco, L. F. Brown, M. Skobe, L. Richard, L. Riccardi, J. Lawler, and M. Detmar Overexpression of Thrombospondin-1 Decreases Angiogenesis and Inhibits the Growth of Human Cutaneous Squamous Cell Carcinomas Am. J. Pathol., August 1, 1999; 155(2): 441 - 452. [Abstract] [Full Text] [PDF]

				C. Carlo-Stella, E. Regazzi, G. Sammarelli, S. Colla, D. Garau, A. Gazit, B. Savoldo, D. Cilloni, A. Tabilio, A. Levitzki, et al. Effects of the Tyrosine Kinase Inhibitor AG957 and an Anti-Fas Receptor Antibody on CD34+ Chronic Myelogenous Leukemia Progenitor Cells Blood, June 1, 1999; 93(11): 3973 - 3982. [Abstract] [Full Text] [PDF]

				A. Sahni, L. A. Sporn, and C. W. Francis Potentiation of Endothelial Cell Proliferation by Fibrin(ogen)-bound Fibroblast Growth Factor-2 J. Biol. Chem., May 21, 1999; 274(21): 14936 - 14941. [Abstract] [Full Text] [PDF]

				F. Madeo, E. Frohlich, M. Ligr, M. Grey, S. J. Sigrist, D. H. Wolf, and K.-U. Frohlich Oxygen Stress: A Regulator of Apoptosis in Yeast J. Cell Biol., May 17, 1999; 145(4): 757 - 767. [Abstract] [Full Text] [PDF]

				C. Menge, L. H. Wieler, T. Schlapp, and G. Baljer Shiga Toxin 1 from Escherichia coli Blocks Activation and Proliferation of Bovine Lymphocyte Subpopulations In Vitro Infect. Immun., May 1, 1999; 67(5): 2209 - 2217. [Abstract] [Full Text] [PDF]

				J. Ramdas, W. Liu, and J. M. Harmon Glucocorticoid-induced Cell Death Requires Autoinduction of Glucocorticoid Receptor Expression in Human Leukemic T Cells Cancer Res., March 1, 1999; 59(6): 1378 - 1385. [Abstract] [Full Text] [PDF]

				J. D. Fortenberry, M. L. Owens, and L. A. S. Brown S-nitrosoglutathione enhances neutrophil DNA fragmentation and cell death Am J Physiol Lung Cell Mol Physiol, March 1, 1999; 276(3): L435 - L442. [Abstract] [Full Text] [PDF]

				L. Mologni, I. Ponzanelli, F. Bresciani, G. Sardiello, D. Bergamaschi, M. Gianni, U. Reichert, A. Rambaldi, M. Terao, and E. Garattini The Novel Synthetic Retinoid 6-[3-adamantyl-4-hydroxyphenyl]-2-naphthalene Carboxylic Acid (CD437) Causes Apoptosis in Acute Promyelocytic Leukemia Cells Through Rapid Activation of Caspases Blood, February 1, 1999; 93(3): 1045 - 1061. [Abstract] [Full Text] [PDF]

				D. A. Persons, J. A. Allay, E. R. Allay, R. A. Ashmun, D. Orlic, S. M. Jane, J. M. Cunningham, and A. W. Nienhuis Enforced Expression of the GATA-2 Transcription Factor Blocks Normal Hematopoiesis Blood, January 15, 1999; 93(2): 488 - 499. [Abstract] [Full Text] [PDF]

				I Korichneva and U Hammerling F-actin as a functional target for retro-retinoids: a potential role in anhydroretinol-triggered cell death J. Cell Sci., January 8, 1999; 112(15): 2521 - 2528. [Abstract] [PDF]