A new method to detect apoptosis in paraffin sections: in situ end- labeling of fragmented DNA

JH Wijsman, RR Jonker, R Keijzer, CJ van de Velde, CJ Cornelisse and JH van Dierendonck

Department of Surgery, University Hospital, Leiden, The Netherlands.

Apoptosis (programmed cell death) can be difficult to detect in routine histological sections. Since extensive DNA fragmentation is an important characteristic of this process, visualization of DNA breaks could greatly facilitate the identification of apoptotic cells. We describe a new staining method for formalin-fixed, paraffin-embedded tissue sections that involves an in situ end-labeling (ISEL) procedure. After protease treatment to permeate the tissue sections, biotinylated nucleotides are in situ incorporated into DNA breaks by polymerase and subsequently stained with DAB via peroxidase-conjugated avidin. Staining of cells with the morphological characteristics of apoptosis was demonstrated in tissues known to exhibit programmed cell death, i.e., prostate and uterus after castration, tumors, lymph node follicles, and embryos. Apoptotic cells could be discriminated morphologically from areas of labeled necrotic cells, in which DNA degradation also occurs. Because apoptosis is relatively easily recognized in H&E-stained sections of involuting prostates of castrated rats, we used this model system to validate the ISEL method for the quantification of apoptotic cells. A high correlation was found between the fractions of ISEL-labeled cells and the fractions of apoptotic cells that were morphologically determined in adjacent sections. We conclude that ISEL is a useful technique for quantification of apoptosis in paraffin sections, especially for those tissues in which morphological determination is difficult. Furthermore, this new staining method enables the use of automated image cytometry for evaluating apoptosis.

Volume 41, Issue 1, pp. 7-12, 01/01/1993
Copyright © 1993 by The Histochemical Society

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				K. W. Bayles, C. A. Wesson, L. E. Liou, L. K. Fox, G. A. Bohach, and W. R. Trumble Intracellular Staphylococcus aureus Escapes the Endosome and Induces Apoptosis in Epithelial Cells Infect. Immun., January 1, 1998; 66(1): 336 - 342. [Abstract] [Full Text] [PDF]

				A. P. Sinha Hikim, C. Wang, Y. Lue, L. Johnson, X.-H Wang, and R. S. Swerdloff Spontaneous Germ Cell Apoptosis in Humans: Evidence for Ethnic Differences in the Susceptibility of Germ Cells to Programmed Cell Death J. Clin. Endocrinol. Metab., January 1, 1998; 83(1): 152 - 156. [Abstract] [Full Text]

				Y.-J. Geng, L. E. Henderson, E. B. Levesque, M. Muszynski, and P. Libby Fas Is Expressed in Human Atherosclerotic Intima and Promotes Apoptosis of Cytokine-Primed Human Vascular Smooth Muscle Cells Arterioscler Thromb Vasc Biol, October 1, 1997; 17(10): 2200 - 2208. [Abstract] [Full Text]

				B. G. Short, D. M. Zimmerman, and L. W. Schwartz Automated Double Labeling of Proliferation and Apoptosis in Glutathione S-transferase-positive Hepatocytes in Rats J. Histochem. Cytochem., September 1, 1997; 45(9): 1299 - 1306. [Abstract] [Full Text] [PDF]

				T. Bellido, V. Z. C. Borba, P. Roberson, and S. C. Manolagas Activation of the Janus Kinase/STAT (Signal Transducer and Activator of Transcription) Signal Transduction Pathway by Interleukin-6-Type Cytokines Promotes Osteoblast Differentiation Endocrinology, September 1, 1997; 138(9): 3666 - 3676. [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]

				N. Katada, R. A. Hinder, T. C. Smyrk, N. Hirabayashi, G. Perdikis, R. J. Lund, T. Woodward, and P. J. Klingler Apoptosis Is Inhibited Early in the Dysplasia-Carcinoma Sequence of Barrett Esophagus Arch Surg, July 1, 1997; 132(7): 728 - 733. [Abstract] [PDF]

				K H Kaestner, D G Silberg, P G Traber, and G Schutz The mesenchymal winged helix transcription factor Fkh6 is required for the control of gastrointestinal proliferation and differentiation. Genes & Dev., June 15, 1997; 11(12): 1583 - 1595. [Abstract] [PDF]

				M. Tagaya, K.-F. Liu, B. Copeland, D. Seiffert, R. Engler, J. H. Garcia, and G. J. del Zoppo DNA Scission After Focal Brain Ischemia : Temporal Differences in Two Species Stroke, June 1, 1997; 28(6): 1245 - 1254. [Abstract] [Full Text]

				F. Rauch, B. Polzar, H. Stephan, S. Zanotti, R. Paddenberg, and H. G. Mannherz Androgen Ablation Leads to an Upregulation and Intranuclear Accumulation of Deoxyribonuclease I in Rat Prostate Epithelial Cells Paralleling Their Apoptotic Elimination J. Cell Biol., May 19, 1997; 137(4): 909 - 923. [Abstract] [Full Text] [PDF]

				S. Krajewski, R. D. Gascoyne, J. M. Zapata, M. Krajewska, S. Kitada, M. Chhanabhai, D. Horsman, K. Berean, L. D. Piro, I. Fugier-Vivier, et al. Immunolocalization of the ICE/Ced-3-Family Protease, CPP32 (Caspase-3), in Non-Hodgkin's Lymphomas, Chronic Lymphocytic Leukemias, and Reactive Lymph Nodes Blood, May 15, 1997; 89(10): 3817 - 3825. [Abstract] [Full Text] [PDF]

				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]

				J. Slomp, A. C. Gittenberger-de Groot, M. A. Glukhova, J. C. van Munsteren, M. M. Kockx, S. M. Schwartz, and V. E. Koteliansky Differentiation, Dedifferentiation, and Apoptosis of Smooth Muscle Cells During the Development of the Human Ductus Arteriosus Arterioscler Thromb Vasc Biol, May 1, 1997; 17(5): 1003 - 1009. [Abstract] [Full Text]

				J. Frade, P Bovolenta, J. Martinez-Morales, A Arribas, J. Barbas, and A Rodriguez-Tebar Control of early cell death by BDNF in the chick retina Development, January 9, 1997; 124(17): 3313 - 3320. [Abstract] [PDF]

				D. A Hilton, S. Love, and R. Barber Demonstration of Apoptotic Cells in Tissue Sections by In Situ Hybridization Using Digoxigenin-labeled Poly(A) Oligonucleotide Probes to Detect Thymidine-rich DNA Sequences J. Histochem. Cytochem., January 1, 1997; 45(1): 13 - 20. [Abstract] [Full Text] [PDF]

				J. Narula, N. Haider, R. Virmani, T. G. DiSalvo, F. D. Kolodgie, R. J. Hajjar, U. Schmidt, M. J. Semigran, G. W. Dec, and B.-A. Khaw Apoptosis in Myocytes in End-Stage Heart Failure N. Engl. J. Med., October 17, 1996; 335(16): 1182 - 1189. [Abstract] [Full Text] [PDF]

				J. B. Grinspan, M. A. Marchionni, M. Reeves, M. Coulaloglou, and S. S. Scherer Axonal Interactions Regulate Schwann Cell Apoptosis in Developing Peripheral Nerve: Neuregulin Receptors and the Role of Neuregulins J. Neurosci., October 1, 1996; 16(19): 6107 - 6118. [Abstract] [Full Text] [PDF]

				M. M. Kockx, G. R.Y. De Meyer, H. Bortier, N. de Meyere, J. Muhring, A. Bakker, W. Jacob, L. Van Vaeck, and A. Herman Luminal Foam Cell Accumulation Is Associated With Smooth Muscle Cell Death in the Intimal Thickening of Human Saphenous Vein Grafts Circulation, September 15, 1996; 94(6): 1255 - 1262. [Abstract] [Full Text]

				A. A. Constan, S. A. Benjamin, J. D. Tessari, D. C. Baker, and R. S.H. Yang Increased Rate of Apoptosis Correlates with Hepatocellular Proliferation in Fischer-344 Rats Following Long-Term Exposure to a Mixture of Groundwater Contaminants Toxicol Pathol, May 1, 1996; 24(3): 315 - 322. [Abstract] [PDF]

				B. Bjorkerud and S. Bjorkerud Contrary Effects of Lightly and Strongly Oxidized LDL With Potent Promotion of Growth Versus Apoptosis on Arterial Smooth Muscle Cells, Macrophages, and Fibroblasts Arterioscler Thromb Vasc Biol, March 1, 1996; 16(3): 416 - 424. [Abstract] [Full Text]

				A. Blaschke, K Staley, and J Chun Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex Development, January 4, 1996; 122(4): 1165 - 1174. [Abstract] [PDF]

				T. L. Goldsworthy, R. Fransson-Steen, and R. R. Maronpot Importance of and Approaches to Quantification of Hepatocyte Apoptosis Toxicol Pathol, January 1, 1996; 24(1): 24 - 35. [Abstract] [PDF]

				J. J. Lysiak, I. M. Hussaini, D. J. Webb, W. F. Glass , II, M. Allietta, and S. L. Gonias alpha(2)-Macroglobulin Functions as a Cytokine Carrier to Induce Nitric Oxide Synthesis and Cause Nitric Oxide-dependent Cytotoxicity in the RAW 264.7 Macrophage Cell Line J. Biol. Chem., September 15, 1995; 270(37): 21919 - 21927. [Abstract] [Full Text] [PDF]

				S. Levin A Toxicologic Pathologist's View of Apoptosis or I Used to Call It Necrobiosis, but Now I'm Singing the Apoptosis Blues Toxicol Pathol, July 1, 1995; 23(4): 533 - 539. [PDF]

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