248:
different mechanisms in different cell types, and the kinetics of these events vary widely, from only a few minutes to several days depending on the cell system. The presence or absence of particular apoptotic event(s), including DNA fragmentation, depends on the "time window" at which the kinetic process of apoptosis is being investigated. Often this may complicate identification of apoptotic cells if cell populations are analyzed only at a single time point e.g. after induction of apoptosis.
2059:
2047:
312:, using cells exposed to widely differing types of trauma, found that during cell death, degraded DNA in "every case had a modal value of between 10(x6) and 10(x7) Dalton and cellular metabolism is required to produce degradation of DNA". However, this observation was without indication of "whether the incision attack on the DNA molecule was a random or rather at a particular site, that have structural or functional meaning". In 1976,
82:
25:
193:
351:
presented a paper revealing that glucocorticoid-induced DNA degradation in rat lymphoid tissue, thymus, and spleen occurred in a specific pattern producing fragments of DNA that were electrophoretically similar to those observed after treatment of chromatin with microccoccal nuclease, which indicated
359:
reported additional evidence for an internucleosomal DNA cleavage pattern as a specific feature of glucocorticoid-treated thymocytes undergoing apoptosis. The internucleosomal DNA cleavage pattern was observed as a specific feature of apoptosis in 1978/1980 and has become a recognised hallmark of
238:
Degradation of nuclear DNA into nucleosomal units is one of the hallmarks of apoptotic cell death. It occurs in response to various apoptotic stimuli in a wide variety of cell types. Molecular characterization of this process identified a specific DNase (CAD, caspase-activated DNase) that cleaves
243:
for CAD and is found complexed with ICAD in proliferating cells. When cells are induced to undergo apoptosis, caspase 3 cleaves ICAD to dissociate the CAD:ICAD complex, allowing CAD to cleave chromosomal DNA. Cells that lack ICAD or that express caspase-resistant mutant ICAD thus do not show DNA
247:
Even though much work has been performed on the analysis of apoptotic events, little information is available to link the timing of morphological features at the cell surface and in the nucleus to the biochemical degradation of DNA in the same cells. Apoptosis can be initiated by a myriad of
597:
Gorczyca, W; Bruno, S; Darzynkiewicz, R; Gong, J; Darzynkiewicz, Z (Nov 1992). "DNA strand breaks occurring during apoptosis - their early insitu detection by the terminal deoxynucleotidyl transferase and nick translation assays and prevention by serine protease inhibitors".
300:, during the study of subchromatin structure, found that chromatin is accessible to the Ca/Mg endonuclease, resulting in the formation of a digestion product with a regular series of molecular weight similar to the one previously described by Williamson (1970). In 1974,
352:
internucleosomal cleavage pattern of DNA degradation occurred during apoptosis. Thus, the first link between programmed cell death/apoptosis and internucleosomal fragmentation of chromatin DNA was discovered and soon became as a specific feature of apoptosis.
392:
shows that DNA fragmentation within individual cells is discontinuous likely reflecting different levels of restriction in accessibility of DNA to DNase, by the supranucleosomal and nucleosomal levels of chromatin structure. The presence of apoptotic
256:
The discovery of the internucleosomal fragmentation of genomic DNA to regular repeating oligonucleosomal fragments generated by Ca/Mg-dependent endonuclease is accepted as one of the best-characterized biochemical markers of
383:
is most frequently used to detect apoptotic DNA fragmentation. Analysis of DNA content by flow cytometry can identify apoptotic cells with fragmented DNA as the cells with fractional DNA content, often called the
432:-phase position. The avidin-peroxidase labeling TUNEL assay is applicable for light absorption microscopy. Many TUNEL-related kits are commercially available. Apoptotic DNA fragmentation is also analyzed using
1099:
682:
Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C (3 June 1991). "A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry".
1520:
Pandey, S.; Walker, P. R.; Sikorska, M. (1994). "Separate pools of endonuclease activity are responsible for internucleosomal and high molecular mass DNA fragmentation during apoptosis".
331:
Six years passed from 1972 to 1978/1980 until the discovery and evaluation of internucleosomal fragmentation of DNA during apoptotic cell death as a hallmark of apoptosis. Since 1972 (
684:
127: (bp) and multiples thereof (360, 540 etc.). The apoptotic DNA fragmentation is being used as a marker of apoptosis and for identification of apoptotic cells either via the
815:
Williamson, Robert (1970-07-14). "Properties of
Rapidly Labeled Deoxyribonucleic Acid Fragments Isolated from the Cytoplasm of Primary Cultures of Embryonic Mouse Liver Cells".
764:
Nagata, S.; Enari, M.; Sakahira, H.; Yokoyama, H.; Okawa, K.; Iwamatsu, A. (1998). "A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD".
268:
described that cytoplasmic DNA isolated from mouse liver cells after culture was characterized by DNA fragments with a molecular weight consisting of multiples of 135
1614:
975:
Williams, Jerry R.; Little, John B.; Shipley, William U. (1974-12-20). "Association of mammalian cell death with a specific endonucleolytic degradation of DNA".
1580:
413:
cells. Treatment of cells with detergent, prior or concurrently with DNA fluorochrome, also reveals DNA fragmentation by virtue of the presence of the sub-G
1549:
Muñoz, E.; Marcos, A.; Unzaga, M. T. (1981). "Effect of protein deficiency on the lysosomal enzyme activities of the spleen and thymus of weanling rats".
932:
1093:
Zakharyan, R. A.; Pogosyan, R. G. (1978). "Glucocorticoid induction of the degradation of lymphocyte chromatin DNA into regularly repeating fragments
1607:
1347:
1302:
235:, the core proteins of the nucleosomes. The linker sites are the only parts of the DNA strand that are exposed and thus accessible to CAD.
50:
409:
apoptotic cells may not be detected with this approach because their fractional DNA content may overlap with that of the non-apoptotic G
272:. This finding was consistent with the hypothesis that these DNA fragments were a specific degradation product of nuclear DNA. In 1972,
1226:
Wlodkowic, D; Telford, W; Skommer, J; Darzynkiewicz, Z (2011). "Apoptosis and Beyond: Cytometry in
Studies of Programmed Cell Death".
239:
chromosomal DNA in a caspase-dependent manner. CAD is synthesized with the help of ICAD (inhibitor of CAD), which works as a specific
482:
Sakahira, H; Enari, M; Nagata, S (January 1998). "Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis".
1984:
1298:"Detection of DNA fragmentation in apoptosis: application of in situ nick translation to cell culture systems and tissue sections"
930:(1973-05-15). "Chromatin sub-structure. The digestion of chromatin DNA at regularly spaced sites by a nuclear deoxyribonuclease".
1676:
1600:
365:
1578:
Varela P, Marcos A, Rey de Viñas JL (1985). "Effect of cortisol treatment in pregnant rats, on cellular growth of progeny".
536:
Wyllie AH (1980-04-10). "Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation".
1187:"Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete "sub-G1" peaks on DNA content histograms"
167:
1959:
1491:
Walker, P. R.; Sikorska, M. (1994). "Endonuclease activities, chromatin structure, and DNA degradation in apoptosis".
1243:
68:
719:
Riccardi C, Nicoletti I (9 November 2006). "Analysis of apoptosis by propidium iodide staining and flow cytometry".
448:, on the other hand, is usually characterized by random DNA fragmentation which forms a "smear" on agarose gels.
1949:
1749:
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Ceskova, M.; Matyásová, J; Cejková, M (1976-12-31). "DNA in chromatin of irradiated lymphoid tissues degrades
1964:
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programmed cell death since then. In 1992 Gorczyca et al. and
Gavrieli et al. independently described the
1840:
1435:
Corcoran, G.; Fix, L.; Jones, D. P.; Moslen, M. T.; Nicotera, P.; Oberhammer, F. A.; Buttyan, R. (1994).
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40:
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635:"Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation"
343:), it is accepted that glucocorticoid-induced death of lymphocytes is a form of apoptosis. In 1978,
1997:
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fragmentation during apoptosis, although they do exhibit some other features of apoptosis and die.
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and distinguished this type of cell death from necrosis based on morphological features. In 1973,
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457:
220:
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120:
119:, particularly the caspase-3 activated DNase (CAD), with subsequent cleavage of nuclear DNA into
1883:
1653:
1470:
Walker, P. R.; Pandey, S.; Sikorska, M. (1995). "Degradation of chromatin in apoptotic cells".
2085:
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2002:
1924:
1878:
1865:
1772:
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112:
869:"Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics"
428:, correlates the detection of DNA strand breaks with the cellular DNA content and thus with
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Gold R, Schmied M, Rothe G, Zischler H, Breitschopf H, Wekerle H, Lassmann H (July 1993).
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372:) which become one of the standard methods to detect and identify apoptotic cells.
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at ~180-bp intervals. This is because the DNA is normally tightly wrapped around
140:
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described internucleosomal fragmentation of irradiated lymphoid chromatin DNA
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Collins JA, Schandi CA, Young KK, Vesely J, Willingham MC (July 1997).
1138:"Cytotoxic Activity of Herbal Medicines as Assessed in Vitro: A Review"
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CODEN: DANAAW, CAN 90:115643 AN 1979:115643 CAPLUS (Copyright 2003 ACS)
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207:(coloured). In apoptotic DNA fragmentation, the DNA is cleaved in the
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1230:. Methods in Cell Biology. Vol. 103. Elsevier. pp. 55–98.
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135:, or the by detection of cells with fractional DNA content ("sub G
433:
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1228:
Recent
Advances in Cytometry, Part B - Advances in Applications
1185:
Kajstura, M; Halicka, HD; Pryjma, J; Darzynkiewicz, Z (2007).
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Gavanji S, Bakhtari A, Famurewa AC, Othman EM (January 2023).
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151:
The enzyme responsible for apoptotic DNA fragmentation is the
1135:
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but not after fixation in the crosslinking fixatives such as
369:
115:. Apoptosis is characterized by the activation of endogenous
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cells. The flow-cytometric assay utilizing the fluorochrome
763:
139:
cells") on DNA content frequency histograms e.g. as in the
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269:
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Apoptotic DNA fragmentation can also be detected by the
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cells or cell fragments, as defined by
Nicoletti et al.
189:, cleaves ICAD and thus causes CAD to become activated.
1035:
1622:
1434:
1343:"Major DNA fragmentation is a late event in apoptosis"
974:
633:
Gavrieli, Y.; Sherman, Y.; Ben-Sasson, S. A. (1992).
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424:. The fluorochrome-based TUNEL assay applicable for
185:. During apoptosis, the apoptotic effector caspase,
166:. CAD is normally inhibited by another protein, the
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481:
397:cells" can also be detected in cells pre-fixed in
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16:Cleavage of DNA into tiny pieces during apoptosis
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1437:"Apoptosis: Molecular Control Point in Toxicity"
862:
85:Apoptotic DNA fragmentation, visualised by the
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1126:Chemical Abstracts v.90,1979;90:115643n p.112.
925:
227:, protein-containing structures that occur in
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1389:(2000-04-10). "Apoptotic DNA fragmentation".
1348:Journal of Histochemistry & Cytochemistry
1303:Journal of Histochemistry & Cytochemistry
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200:, consisting of DNA (grey) wrapped around a
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69:Learn how and when to remove this message
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100:DNA (right) are included for comparison.
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442:"ladder" pattern at ~180-BP intervals
366:terminal deoxynucleotidyl transferase
211:region, which is the part of the DNA
1100:Doklady Akademii Nauk Armyanskoi SSR
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1441:Toxicology and Applied Pharmacology
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867:; Currie, Alastair (August 1972).
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685:Journal of Immunological Methods
49:has been specified. Please help
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1142:Chemistry & Biodiversity
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831:10.1016/0022-2836(70)90277-9
818:Journal of Molecular Biology
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215:wrapped around the histones.
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1040:into regular fragments".
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261:(programmed cell death).
123:fragments of roughly 180
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1639:Outline of cell biology
458:Caspase-activated DNase
221:internucleosomal linker
209:internucleosomal linker
1563:10.1093/jn/111.12.2133
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1405:10.1006/excr.2000.4834
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2003:In situ hybridization
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1915:monoclonal antibodies
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252:Historical background
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113:programmed cell death
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1965:Molecular biologists
1740:Clone (cell biology)
1581:IRCS Medical Science
1317:10.1177/41.7.8515045
1204:10.1002/cyto.a.20357
107:is a key feature of
51:improve this article
39:to meet Knowledge's
1950:Biochemistry topics
1851:Population genetics
1826:Genetic engineering
1735:Signal transduction
1672:Genetic engineering
991:1974Natur.252..754W
887:10.1038/bjc.1972.33
778:1998Natur.391...43E
612:10.3892/ijo.1.6.639
552:1980Natur.284..555W
496:1998Natur.391...96S
219:CAD cleaves DNA at
1841:Molecular genetics
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928:Burgoyne, Leigh A.
863:Kerr, John F. R.;
405:. The late-S and G
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1937:Molecular biology
1821:Genetic disorders
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926:Hewish, Dean R.;
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440:to demonstrate a
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865:Wyllie, Andrew
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1961:
1958:
1956:
1953:
1951:
1948:
1946:
1943:
1942:
1940:
1938:
1934:
1926:
1923:
1921:
1918:
1916:
1913:
1912:
1910:
1907:
1905:
1902:
1900:
1897:
1895:
1892:
1890:
1887:
1885:
1884:Extremophiles
1882:
1880:
1877:
1875:
1872:
1871:
1869:
1867:
1863:
1857:
1854:
1852:
1849:
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1827:
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1809:
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1654:Biotechnology
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1523:
1518:
1514:
1510:
1506:
1502:
1498:
1494:
1489:
1485:
1481:
1478:(2): 97–104.
1477:
1473:
1468:
1464:
1460:
1455:
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1446:
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1438:
1433:
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1422:
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1245:9780123854933
1241:
1237:
1233:
1229:
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1214:
1210:
1205:
1200:
1197:(3): 125–31.
1196:
1192:
1188:
1181:
1173:
1169:
1165:
1161:
1156:
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1147:
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1139:
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1123:
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1049:
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1024:
1020:
1016:
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979:
971:
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929:
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905:
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840:
836:
832:
828:
824:
820:
819:
811:
803:
799:
795:
791:
787:
786:10.1038/34112
783:
779:
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771:
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728:
724:
723:
715:
707:
703:
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666:
661:
656:
652:
648:
644:
640:
636:
629:
621:
617:
613:
609:
606:(6): 639–48.
605:
601:
593:
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569:
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561:
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505:
504:10.1038/34214
501:
497:
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463:DNA laddering
461:
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439:
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431:
427:
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404:
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329:
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206:
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194:
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188:
184:
182:
178:
174:
170:
165:
163:
159:
155:
144:
142:
134:
130:
129:DNA laddering
126:
122:
118:
117:endonucleases
114:
110:
106:
99:
96:(middle) and
95:
92:
88:
87:DNA laddering
83:
73:
70:
62:
59:February 2012
52:
48:
42:
38:
37:
30:
21:
20:
2086:Cell biology
2064:Cell biology
2062:
2050:
2033:Western blot
1955:Biomolecules
1879:Bacteriology
1866:Microbiology
1773:Gastrulation
1720:Cytoskeleton
1697:Cell biology
1628:cell biology
1585:
1579:
1554:
1550:
1525:
1521:
1496:
1492:
1475:
1471:
1444:
1440:
1399:(1): 12–18.
1396:
1390:
1352:
1346:
1307:
1301:
1227:
1221:
1194:
1190:
1180:
1145:
1141:
1131:
1122:
1104:
1098:
1094:
1088:
1047:
1043:FEBS Letters
1041:
1037:
1031:
982:
976:
970:
937:
931:
921:
878:
872:
822:
816:
810:
769:
765:
759:
726:
720:
714:
689:
683:
677:
642:
638:
628:
603:
599:
592:
543:
537:
487:
483:
477:
419:
403:formaldehyde
379:
354:
330:
325:
287:
263:
255:
246:
237:
218:
212:
180:
176:
172:
171:nhibitor of
168:
161:
157:
153:
150:
111:, a type of
104:
103:
65:
56:
33:
2013:Microscopes
1945:Biochemists
1874:Antibiotics
1836:Geneticists
1811:Chromosomes
1783:Neurulation
1687:Vaccination
1191:Cytometry A
1148:(2): 3–27.
600:Int J Oncol
422:TUNEL assay
225:nucleosomes
183:Nase (ICAD)
133:TUNEL assay
131:assay, the
53:if you can.
2080:Categories
1909:Immunology
1788:Teratogens
1768:Morphogens
1763:Embryology
1725:Organelles
1705:Cell cycle
1682:Stem cells
1588:: 412–413.
469:References
430:cell cycle
266:Williamson
198:nucleosome
164:Nase (CAD)
125:base pairs
2096:Apoptosis
1413:0014-4827
1371:0022-1554
1326:0022-1554
1282:ignored (
1272:cite book
1172:255473013
1113:0366-8606
1064:0014-5793
1007:0028-0836
954:0006-291X
895:0007-0920
839:0022-2836
568:0028-0836
355:In 1980,
345:Zakharyan
318:Matyasova
288:apoptosis
264:In 1970,
259:apoptosis
241:chaperone
229:chromatin
187:caspase-3
179:ctivated
160:ctivated
147:Mechanism
109:apoptosis
1975:Proteins
1970:Peptides
1904:Virology
1899:Mycology
1846:Mutation
1798:Genetics
1484:17180071
1421:10739646
1264:21722800
1213:17252584
1164:36595710
1072:16386038
743:17406435
620:21584593
452:See also
446:Necrosis
349:Pogosyan
302:Williams
297:Burgoyne
233:histones
205:tetramer
34:require
1993:Cloning
1667:Cloning
1571:7310538
1542:7654336
1513:7654335
1463:7940532
1379:9212818
1334:8515045
1255:3263828
1095:in vivo
1038:in vivo
1023:4181803
1015:4474604
987:Bibcode
962:4711166
913:4561027
904:2008650
847:5481278
802:4407426
794:9422506
774:Bibcode
751:4469406
706:1710634
669:1400587
660:2289665
584:4318802
576:6245367
548:Bibcode
520:4329685
512:9422513
492:Bibcode
434:agarose
399:ethanol
326:in vivo
322:Cejkova
310:Shipley
202:histone
175:aspase
156:aspase-
98:control
36:cleanup
1758:Ageing
1569:
1540:
1511:
1482:
1461:
1419:
1411:
1377:
1369:
1332:
1324:
1262:
1252:
1242:
1211:
1170:
1162:
1111:
1080:579849
1078:
1070:
1062:
1021:
1013:
1005:
978:Nature
960:
952:
911:
901:
893:
845:
837:
800:
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766:Nature
749:
741:
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667:
657:
618:
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574:
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539:Nature
518:
510:
484:Nature
393:"sub-G
357:Wyllie
341:Currie
339:, and
337:Wyllie
320:, and
314:Scalka
308:, and
306:Little
292:Hewish
284:Currie
282:, and
279:Wyllie
94:marker
1889:Fungi
1831:Genes
1715:Cells
1168:S2CID
1076:S2CID
1019:S2CID
798:S2CID
747:S2CID
580:S2CID
516:S2CID
384:sub-G
370:TUNEL
1626:and
1567:PMID
1538:PMID
1509:PMID
1480:PMID
1459:PMID
1417:PMID
1409:ISSN
1375:PMID
1367:ISSN
1330:PMID
1322:ISSN
1284:help
1260:PMID
1240:ISBN
1209:PMID
1160:PMID
1109:ISSN
1068:PMID
1060:ISSN
1011:PMID
1003:ISSN
958:PMID
950:ISSN
909:PMID
891:ISSN
843:PMID
835:ISSN
790:PMID
739:PMID
702:PMID
665:PMID
616:PMID
572:PMID
564:ISSN
508:PMID
436:gel
347:and
333:Kerr
294:and
274:Kerr
91:1 kb
2101:DNA
1856:RNA
1816:DNA
1559:doi
1555:111
1530:doi
1501:doi
1449:doi
1445:128
1401:doi
1397:256
1357:doi
1312:doi
1250:PMC
1232:doi
1199:doi
1150:doi
1097:".
1052:doi
995:doi
983:252
942:doi
899:PMC
883:doi
827:doi
782:doi
770:391
731:doi
694:doi
690:139
655:PMC
647:doi
643:119
608:doi
556:doi
544:284
500:doi
488:391
270:kDa
213:not
45:No
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