Morphological and cytochemical determination of cell death by apoptosis

Histochemistry and Cell Biology

Volumn 129, Issue 1, 2008, Pages 33-43

  Taatjes, Douglas J ^a,b   Sobel, Burton E ^a   Budd, Ralph C ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Cell death; Cytochemistry; Immunostaining; Microscopy; Morphology

Indexed keywords

LIPOCORTIN 5;

APOPTOSIS; ATOMIC FORCE MICROSCOPY; CELL DEATH; CELL STRUCTURE; CYTOCHEMISTRY; ELECTRON MICROSCOPY; HEART; HUMAN; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; APOPTOSIS; HUMANS; MICROSCOPY;

EID: 37449028923     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-007-0356-9     Document Type: Review

References (67)

1. Abbate A, De Falco M, Morales C, Gelpi R, Prisco M, De Luca A, Palleiro J, Fedele V, Feroce F, Baldi F, Vetrovec GW, Baldi A (2007) Electron microscopy characterization of cardiomyocyte apoptosis in ischemic heart disease. Int J Cardiol 114:118-120
2. Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322-1326
3. Barrett KL, Willingham JM, Garvin AJ, Willingham MC (2001) Advances in cytochemical methods for detection of apoptosis. J Histochem Cytochem 49:821-832
4. Bedner E, Li X, Gorczyca W, Melamed MR, Darzynkiewicz Z (1999) Analysis of apoptosis by laser scanning cytometry. Cytometry 35:181-195
5. Bilyy RO, Stoika RS (2003) Lectinocytochemical detection of apoptotic murine leukemia L1210 cells. Cytometry A 56A:89-95
6. Bilyy RO, Antonyuk VO, Stoika RS (2004) Cytochemical study of role of α-d-mannose- and β-d-galactose-containing glycoproteins in apoptosis. J Mol Histol 35:829-838
7. Bilyy R, Kit Y, Hellman U, Tryndyak V, Kaminskyy V, Stoika R (2005) In vivo expression and characteristics of novel α-d-mannose-rich glycoprotein markers of apoptotic cells. Cell Biol Int 29:920-928
8. Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phy Rev Lett 56:930-933
9. Buder-Hoffman S, Palmer C, Vacek P, Taatjes D, Mossman B (2001) Different accumulation of activated extracellular signal-regulated kinases (ERK1/2) and role in cell-cycle alterations by epidermal growth factor, hydrogen peroxide, or asbestos in pulmonary epithelial cells. Am J Respir Cell Mol Biol 24:405-413
10. Cain K, Bratton SB, Langlais C, Walker G, Brown DG, Sun XM, Cohen GM (2000) Apaf-1 oligomerizes into biologically active approximately 700-kDa and inactive approximately 1.4-MDa apoptosome complexes. J Biol Chem 275:6067-6070
11. Chun HJ, Zheng L, Ahmad M, Wang J, Speirs CK, Siegel RM, Dale JK, Puck J, Davis J, Hall CG, Skoda-Smith S, Atkinson TP, Straus SE, Lenardo MJ (2002) Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 419:395-399
12. Collins JA, Schandl CA, Young KK, Vesely J, Willingham MC (1997) Major DNA fragmentation is a late event in apoptosis. J Histochem Cytochem 45:923-934
13. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N, Prevost M-C, Leber B, Andrews D, Penninger J, Kroemer G (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 14:729-739
14. Frankfurt OS (1994) Detection of apoptosis in leukemic and breast cancer cells with monoclonal antibody to single-stranded DNA. Anticancer Res 14:1861-1870
15. Frankfurt OS, Krishan A (2001) Identification of apoptotic cells by formamide-induced DNA denaturation in condensed chromatin. J Histochem Cytochem 49:369-378
16. Frankfurt OS, Robb JA, Sugarbaker EV, Villa L (1996) Monoclonal antibody to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. Exp Cell Res 226:387-397
17. Fung H, Kow YW, van Houten B, Taatjes DJ, Hatahet Z, Yanssen YMW, Vacek P, Faux SP, Mossman BT (1998) Asbestos increases mammalian AP-endonuclease gene expression, protein levels, and enzyme activity in mesothelial cells. Cancer Res 58:189-194
18. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G (2007) Cell death modalities: classifications and pathophysiological implications. Cell Death Differ 14:1237-1243
19. Germain F, Fernandez E, De La Villa P (2007) Morphological signs of apoptosis in axotomized ganglion cells of the rabbit retina. Neuroscience 144:898-910
20. Gown AM, Willingham MC (2002) Improved detection of apoptotic cells in archival paraffin sections: immunohistochemistry using antibodies to cleaved caspase 3. J Histochem Cytochem 50:449-454
21. Groos S, Reale E, Luciano L (2003) General suitability of techniques for in situ detection of apoptosis in small intestinal epithelium. Anat Rec 272:503-513
22. Hansma H, Ho J (1994) Biomolecular imaging with the atomic force microscope. Annu Rev Biophys Biomol Struct 23:115-139
23. Hessler JA, Budor A, Putchakayala K, Mecke A, Rieger D, Banaszak Holl MM, Orr BG, Bielinska A, Beals J, Baker J Jr (2005) Atomic force microscopy study of early morphological changes during apoptosis. Langmuir 21:9280-9286
24. Ito Y, Shibata M-A, Kusakabe K, Otsuki Y (2006) Method of specific detection of apoptosis using formamide-induced DNA denaturation assay. J Histochem Cytochem 54:683-692
25. Jiang S, Cai J, Wallace DC, Jones DP (1999) Cytochrome c-mediated apoptosis in cells lacking mitochondrial DNA. Signaling pathway involving release and caspase 3 activation is conserved. J Biol Chem 274:29905-29911
26. Jung M, Davis WP, Taatjes DJ, Churg A, Mossman BT (2000) Asbestos and cigarette smoke cause increased DNA strand breaks and necrosis in bronchiolar epithelial cells in vivo. Free Radic Biol Med 28:1295-1299
27. Jung M, Grunberg S, Timblin C, Buder-Hoffman S, Vacek P, Taatjes DJ, Mossman BT (2004) Paclitaxel and vinorelbine cause synergistic increases in apoptosis but not in microtubular disruption in human lung adenocarcinoma cells (A-549). Histochem Cell Biol 121:115-121
28. Kamentsky LA, Kamentsky LD (1991) Microscope-based multiparameter laser scanning cytometer yielding data comparable to flow cytometry data. Cytometry 12:381-387
29. Kamentsky LA, Burger DE, Gershman RJ, Kamentsky LD, Luther E (1997) Slide-based laser scanning cytometry. Acta Cytol 41:123-143
30. Kanoh M, Takemura G, Misao J, Hayakawa Y, Aoyama T, Nishigaki K, Noda T, Fujiwara T, Fukuda K, Minatoguchi S, Fujiwara H (1999) Significance of myocytes with positive DNA end-labeling (TUNEL) in hearts with dilated cardiomyopathy. Circulation 99:2757-2764
31. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257
32. Kockx MM, Muhring J, Knaapen MW, De Meyer GR (1998) RNA synthesis and splicing interferes with DNA in situ end labeling techniques used to detect apoptosis. Am J Pathol 152:885-888
33. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pasla ST, van Oers MH (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415-1420
34. Krueger A, Fas SC, Baumann S, Krammer PH (2003) The role of CD95 in the regulation of peripheral T-cell apoptosis. Immunol Rev 193:58-69
35. Labat-Moleur F, Guillermet C, Lorimier P, Robert C, Lantuejoul S, Brambilla E, Negoescu A (1998) TUNEL apoptotic cell detection in tissue sections: critical evaluation and improvement. J Histochem Cytochem 46:327-334
36. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501
37. Linette GP, Li Y, Roth K, Korsmeyer SJ (1996) Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proc Natl Acad Sci USA 93:9545-9552
38. Madl J, Rhode S, Stangl H, Stockinger H, Hinterdorfer P, Schutz GJ, Kada G (2006) A combined optical and atomic force microscope for live cell investigations. Ultramicroscopy 106:645-651
39. Maroko PR, Libby P, Sobel BE, Bloor CM, Sybers HD, Shell WE, Covell Jw, Braunwald E (1972) Effect of glucose-insulin-potassium infusion on myocardial infarction following experimental coronary artery occlusion. Circulation 45:1160-1172
40. Montigny WJ, Quinn AS, Wu X-X, Bovill EG, Rand JH, Taatjes DJ (2006) Atomic force microscopy in the study of macromolecular interactions in hemostasis and thrombosis: utility for investigation of the antiphospholipid syndrome. In: Jena BJ, Horber JKH (eds) Force microscopy: applications in biology and medicine, Wiley, Hoboken, pp 267-286
41. Morgan M, Thorburn J, Pandolfi PP, Thorburn A (2002) Nuclear and cytoplasmic shuttling of TRADD induces apoptosis via different mechanisms. J Cell Biol 157:975-984
42. Negoescu A, Lorimier P, Labat-Moleur F, Drouet C, Robert C, Guillermet C, Brambilla C, Brambilla E (1996) In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparation. J Histochem Cytochem 44:959-968
43. Ohno M, Takemura G, Ohno A, Misao J, Hayakawa Y, Minatoguchi S, Fujiwara T, Fujiwara H (1998) Apoptotic myocytes in infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with in situ nick end-labeling. Circulation 98:1422-1430
44. Penaloza C, Lin L, Lockshin RA, Zakeri Z (2006) Cell death in development: shaping the embryo. Histochem Cell Biol 126:149-158
45. Pozarowski P, Holden E, Darzynkiewicz Z (2006) Laser scanning cytometry: principles and applications. In: Taatjes DJ, Mossman BT (eds) Methods in molecular biology. Cell imaging techniques: methods and protocols, vol 319. Humana Press, Totowa, pp 165-192
46. Rand JH, Wu X-X, Quinn AS, Chen PP, McCrae KR, Bovill EG, Taatjes DJ (2003) Human monoclonal antiphospholipid antibodies disrupt the annexin A5 anticoagulant shield on phospholipid bilayers. Evidence from atomic force microscopy and functional assay. Am J Pathol 163:1193-1200
47. Salmena L, Lemmers B, Hakem A, Matysiak-Zablocki E, Murakami K, Au PY, Berry DM, Tamblyn L, Shehabeldin A, Migon E, Wakeham A, Bouchard D, Yeh WC, McGlade JC, Ohashi PS, Hakem R (2003) Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev 17:883-895
48. Shell WE, Sobel BE (1974) Protection of jeopardized ischemic myocardium by reduction of ventricular afterload. N Engl J Med 291:481-486
49. Shukla A, Jung M, Stern M, Fukagawa NK, Taatjes DJ, Sawyer D, van Houten B, Mossman BT (2003) Asbestos induces mitochondrial DNA damage and dysfunction linked to the development of apoptosis. Am J Physiol Lung Cell Mol Physiol 285:L1018-L1025
50. Sloop GD, Roa JC, Delgado AG, Balart JT, Hines MO, Hill JM (1999) Histologic sectioning produces TUNEL reactivity. A potential cause of false-positive staining. Arch Pathol Lab Med 123:529-532
51. Sobel BE, Braunwald E (1980) Management of acute myocardial infarction. In: Braunwald E (ed) Heart disease. WB Saunders, Philadelphia, pp 1353-1386
52. Sobel BE, Tarikuz Zaman AKM, Budd RC, Schneider DJ, Taatjes DJ (2007) Attenuation of apoptosis and the eye of the beholder. Coron Artery Dis (in press)
53. Strasser A (2001) BH3-only members of the Bcl-2 family are critical inducers of apoptosis and preclude autoimmunity. Abstract 003 Keystone Symposium on Molecular Mechanisms of Apoptosis, 16-22 January 2001, Keystone, CO
54. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, Loeffler M, Costantini P, Ferri KF, Irinopoulou T, Prevost M-C, Brothers G, Mak TW, Penninger J, Earnshaw WC, Kroemer G (2000) Two distinct pathways leading to nuclear apoptosis. J Exp Med 192:571-579
55. Taatjes DJ, Quinn AS, Jenny RJ, Hale P, Bovill EG, McDonagh J (1997) Tertiary structure of the hepatic cell protein fibrinogen in fluid revealed by atomic force microscopy. Cell Biol Int 21:715-726
56. Taatjes DJ, Palmer CJ, Pantano C, Buder-Hoffmann S, Cummins A, Mossman BT (2001) Laser-based microscopic approaches: application to cell signaling in environmental lung disease. Biotechniques 31:880-894
57. Taatjes DJ, Wadsworth MP, Tarikuz Zaman AKM, Schneider DJ, Sobel BE (2007) A novel dual staining method for identification of apoptotic cells reveals a modest apoptotic response in infarcted mouse myocardium. Histochem Cell Biol 128:275-283
58. Takemura G, Fujiwara H (2006) Morphological aspects of apoptosis in heart diseases. J Cell Mol Med 10:56-75
59. Tateyama H, Tada T, Hattori H, Murase T, Li WX, Eimoto T (1998) Effects of prefixation and fixation times on apoptosis detection by in situ end-labelling of fragmented DNA. Arch Pathol Lab Med 51:252-253
60. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43-53
61. Walker JA, Quirke P (2001) Viewing apoptosis through a "TUNEL". J Pathol 195:275-276
62. Watanabe M, Hitomi M, van der Wee K, Rothenberg F, Fisher SA, Zucker R, Svoboda KKH, Goldsmith EC, Heiskanen KM, Nieminen A-L (2002) The pros and cons of apoptosis assays for use in the study of cells, tissues, and organs. Microsc Microanal 8:375-391
63. White C, Li C, Yang J, Petrenko NB, Madesh M, Thompson CB, Foskett JK (2005) The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat Cell Biol 7:1021-1028
64. Wikstrom JD, Katzman SM, Mohamed H, Twig G, Graf SA, Heart E, Molina AJ, Corkey BE, de Vargas LM, Danial NN, Collins S, Shirihai OS (2007) Beta-cell mitochondria exhibit membrane potential heterogeneity that can be altered by stimulatory or toxic fuel levels. Diabetes 56:2569-2578
65. Willingham MC (1999) Cytochemical methods for the detection of apoptosis. J Histochem Cytochem 47:1101-1109
66. Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306
67. Yuan Z, Taatjes DJ, Mossman BT, Heintz NH (2004) The duration of nuclear extracellular signal-regulated kinase 1 and 2 signaling during cell cycle reentry distinguishes proliferation from apoptosis in response to asbestos. Cancer Res 64:6530-6536