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American Journal of Pathology, Vol 136, 593-608, Copyright © 1990 by American Society for Investigative Pathology

REGULAR ARTICLES

Apoptosis. The role of the endonuclease

MJ Arends, RG Morris and AH Wyllie
Department of Pathology, University of Edinburgh Medical School, United Kingdom.

Cell death by apoptosis mediates several important physiologic and pathologic processes and appears to be intrinsically programmed. Its characteristic features are distinctive morphologic changes of nucleus and cytoplasm, along with cleavage of chromatin at regularly spaced sites. Here we study DNA organization and nuclear structure in apoptotic thymocytes to define the cleavage event and, by implication, the role of the responsible endonuclease. We show that in apoptosis, double-stranded cleavage of DNA generates two classes of chromatin fragments: 70% of DNA exists as long, H1-rich oligonucleosomes bound to the nucleus, and 30% comprises short oligonucleosomes and mononucleosomes, which are depleted in H1, enriched in HMG1 and 2, and not attached to the nucleus. This minority class probably derives from chromatin in a transcriptionally active configuration, which would allow better access to enzymes in the nucleoplasm, producing more complete digestion. The characteristic nucleolar morphology in apoptosis can also be explained in terms of cleavage of the transcriptionally active ribosomal genes, with conservation of the nucleolin-rich fibrillar center. The chromatin cleavage, nucleolar morphologic changes, and chromatin condensation were closely mimicked by micrococcal nuclease digestion of normal thymocyte nuclei in the presence of protease inhibitors. Thus, in apoptosis, selective activation of an endogenous endonuclease appears to be responsible not only for widespread chromatin cleavage but also for the major nuclear morphologic changes.

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				R. Hayashi, Y. Ito, K. Matsumoto, Y. Fujino, and Y. Otsuki Quantitative Differentiation of Both Free 3'-OH and 5'-OH DNA Ends Between Heat-induced Apoptosis and Necrosis J. Histochem. Cytochem., September 1, 1998; 46(9): 1051 - 1060. [Abstract] [Full Text]

				E. Hanon, G. Meyer, A. Vanderplasschen, C. Dessy-Doize, E. Thiry, and P.-P. Pastoret Attachment but Not Penetration of Bovine Herpesvirus 1 Is Necessary To Induce Apoptosis in Target Cells J. Virol., September 1, 1998; 72(9): 7638 - 7641. [Abstract] [Full Text] [PDF]

				S. A. Back, X. Gan, Y. Li, P. A. Rosenberg, and J. J. Volpe Maturation-Dependent Vulnerability of Oligodendrocytes to Oxidative Stress-Induced Death Caused by Glutathione Depletion J. Neurosci., August 15, 1998; 18(16): 6241 - 6253. [Abstract] [Full Text] [PDF]

				W. Zhu, H. Friedman, and T. W. Klein Delta 9-Tetrahydrocannabinol Induces Apoptosis in Macrophages and Lymphocytes: Involvement of Bcl-2 and Caspase-1 J. Pharmacol. Exp. Ther., August 1, 1998; 286(2): 1103 - 1109. [Abstract] [Full Text]

				L. A. Barber, D. F. Spandau, S. C. Rathman, R. C. Murphy, C. A. Johnson, S. W. Kelley, S. A. Hurwitz, and J. B. Travers Expression of the Platelet-activating Factor Receptor Results in Enhanced Ultraviolet B Radiation-induced Apoptosis in a Human Epidermal Cell Line J. Biol. Chem., July 24, 1998; 273(30): 18891 - 18897. [Abstract] [Full Text] [PDF]

				G. Takemura, M. Ohno, Y. Hayakawa, J. Misao, M. Kanoh, A. Ohno, Y. Uno, S. Minatoguchi, T. Fujiwara, and H. Fujiwara Role of Apoptosis in the Disappearance of Infiltrated and Proliferated Interstitial Cells After Myocardial Infarction Circ. Res., June 15, 1998; 82(11): 1130 - 1138. [Abstract] [Full Text] [PDF]

				L. A. Scheving, W.-H. Jin, K.-M. Chong, W. Gardner, and F. O. Cope Dying enterocytes downregulate signaling pathways converging on Ras: rescue by protease inhibition Am J Physiol Cell Physiol, May 1, 1998; 274(5): C1363 - C1372. [Abstract] [Full Text] [PDF]

				R. Shtrichman and T. Kleinberger Adenovirus Type 5 E4 Open Reading Frame 4 Protein Induces Apoptosis in Transformed Cells J. Virol., April 1, 1998; 72(4): 2975 - 2982. [Abstract] [Full Text] [PDF]

				J. Ya, M. J. B. van den Hoff, P. A. J. de Boer, S. Tesink-Taekema, D. Franco, A. F. M. Moorman, and W. H. Lamers Normal Development of the Outflow Tract in the Rat Circ. Res., March 9, 1998; 82(4): 464 - 472. [Abstract] [Full Text] [PDF]

				F. Labat-Moleur, C. Guillermet, P. Lorimier, C. Robert, S. Lantuejoul, E. Brambilla, and A. Negoescu TUNEL Apoptotic Cell Detection in Tissue Sections: Critical Evaluation and Improvement J. Histochem. Cytochem., March 1, 1998; 46(3): 327 - 334. [Abstract] [Full Text]

				A. Leri, Y. Liu, A. Malhotra, Q. Li, P. Stiegler, P. P. Claudio, A. Giordano, J. Kajstura, T. H. Hintze, and P. Anversa Pacing-Induced Heart Failure in Dogs Enhances the Expression of p53 and p53-Dependent Genes in Ventricular Myocytes Circulation, January 20, 1998; 97(2): 194 - 203. [Abstract] [Full Text] [PDF]

				I. Yamadori, T. Yoshino, E. Kondo, L. Cao, T. Akagi, Y. Matsuo, and J. Minowada Comparison of Two Methods of Staining Apoptotic Cells of Leukemia Cell Lines: Terminal Deoxynucleotidyl Transferase and DNA Polymerase I Reactions J. Histochem. Cytochem., January 1, 1998; 46(1): 85 - 90. [Abstract] [Full Text]

				N. Shirafuji, S. Takahashi, S. Matsuda, and S. Asano Mitochondrial Antisense RNA for Cytochrome C Oxidase (MARCO) Can Induce Morphologic Changes and Cell Death in Human Hematopoietic Cell Lines Blood, December 1, 1997; 90(11): 4567 - 4577. [Abstract] [Full Text] [PDF]

				N. R. Murray and A. P. Fields Atypical Protein Kinase C iota  Protects Human Leukemia Cells against Drug-induced Apoptosis J. Biol. Chem., October 31, 1997; 272(44): 27521 - 27524. [Abstract] [Full Text] [PDF]

				S. A. Capurso, M. E. Calhoun, R. R. Sukhov, P. R. Mouton, D. L. Price, and V. E. Koliatsos Deafferentation Causes Apoptosis in Cortical Sensory Neurons in the Adult Rat J. Neurosci., October 1, 1997; 17(19): 7372 - 7384. [Abstract] [Full Text] [PDF]

				M. E. Mackey, Y. Wu, R. Hu, J. A. DeMaro, M. F. Jacquin, G. K. Kanellopoulos, C. Y. Hsu, and N. T. Kouchoukos Cell Death Suggestive of Apoptosis After Spinal Cord Ischemia in Rabbits Stroke, October 1, 1997; 28(10): 2012 - 2017. [Abstract] [Full Text]

				D. M. Monack, J. Mecsas, N. Ghori, and S. Falkow Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death PNAS, September 16, 1997; 94(19): 10385 - 10390. [Abstract] [Full Text] [PDF]

				A. Tomkinson, J. Reeve, R. W. Shaw, and B. S. Noble The Death of Osteocytes via Apoptosis Accompanies Estrogen Withdrawal in Human Bone J. Clin. Endocrinol. Metab., September 1, 1997; 82(9): 3128 - 3135. [Abstract] [Full Text] [PDF]

				M. Mancini, B. O. Anderson, E. Caldwell, M. Sedghinasab, P. B. Paty, and D. M. Hockenbery Mitochondrial Proliferation and Paradoxical Membrane Depolarization during Terminal Differentiation and Apoptosis in a Human Colon Carcinoma Cell Line J. Cell Biol., July 28, 1997; 138(2): 449 - 469. [Abstract] [Full Text] [PDF]

				J. A. Collins, C. A. Schandl, K. K. Young, J. Vesely, and M. C. Willingham Major DNA Fragmentation Is a Late Event in Apoptosis J. Histochem. Cytochem., July 1, 1997; 45(7): 923 - 934. [Abstract] [Full Text] [PDF]

				E. Ayroldi, G. Migliorati, L. Cannarile, R. Moraca, D. V. Delfino, and C. Riccardi CD2 Rescues T Cells From T-Cell Receptor/CD3 Apoptosis: A Role for the Fas/Fas-L System Blood, May 15, 1997; 89(10): 3717 - 3726. [Abstract] [Full Text] [PDF]

				C. Allera, G. Lazzarini, E. Patrone, I. Alberti, P. Barboro, P. Sanna, A. Melchiori, S. Parodi, and C. Balbi The Condensation of Chromatin in Apoptotic Thymocytes Shows a Specific Structural Change J. Biol. Chem., April 18, 1997; 272(16): 10817 - 10822. [Abstract] [Full Text] [PDF]