Neuronal apoptosis studied by a sequential TUNEL technique: A method for tract-tracing

Brain Research Protocols

Volumn 4, Issue 2, 1999, Pages 140-146

  Hara, Akira ^a   Niwa, Masayuki ^a   Iwai, Tomohiko ^a   Nakashima, Masaya ^a   Bunai, Yasuo ^a   Uematsu, Toshihiko ^a   Yoshimi, Naoki ^a   Mori, Hideki ^a  

^a GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apical dendrite; DAPI; DNA fragmentation; Forebrain ischemia; Tract tracing; TUNEL

Indexed keywords

DNA; DNA FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL DEATH; CELL LABELING; CONTROLLED STUDY; DENDRITE; GERBIL; HIPPOCAMPUS; MALE; NERVE CELL; NERVE FIBER TRANSPORT; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; REGENERATION;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; FLUORESCENT DYES; GERBILLINAE; HIPPOCAMPUS; IN SITU NICK-END LABELING; INDOLES; MALE; NEURONS;

EID: 0032840028     PISSN: 1385299X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1385-299X(99)00012-4     Document Type: Article

References (34)

1. Allen R.T., Hunter W.J. III, Agrawal D.K. Morphological and biochemical characterization and analysis of apoptosis. J. Pharmacol. Toxicol. Methods. 37:1997;215-228.
2. Bardales R.H., Xie S.S., Hsu S.M. In situ DNA fragmentation assay for detection of apoptosis in paraffin-embedded tissue sections. Technical considerations. Am. J. Clin. Pathol. 107:1997;332-336.
3. Collins J.A., Schandi C.A., Young K.K., Vesely J., Willingham M.C. Major DNA fragmentation is a late event in apoptosis. J. Histochem. Cytochem. 45:1997;923-934.
4. Charriaut-Marlangue C., Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 7:1995;61-64.
5. Davison F.D., Groves M., Scaravilli F. The effects of formalin fixation on the detection of apoptosis in human brain by in situ end-labelling of DNA. Histochem. J. 27:1995;983-988.
6. van Domburg P.H., ten Donkelaar H.J. The human substantia nigra and ventral tegmental area. A neuroanatomical study with notes on aging and aging diseases. Adv. Anat. Embryol. Cell Biol. 121:1991;1-132.
7. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
8. Gerfen C.R., Sawchenko P.E. A method for anterograde axonal tracing of chemically specified circuits in the central nervous system: combined Phaseolus vulgaris-leucoagglutinin (PHA-L) tract tracing and immunohistochemistry. Brain Res. 343:1985;144-150.
9. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology. 21:1995;1465-1468.
10. Hara A., Niwa M., Iwai T., Nakashima M., Yano H., Uematsu T., Yoshimi N., Mori H. Transport of fragmented DNA in apical dendrites of gerbil CA1 pyramidal neurons following transient forebrain ischemia. Brain Res. 806:1998;274-277.
11. Hara A., Niwa M., Nakashima M., Iwai T., Uematsu T., Yoshimi N., Mori H. Protective effect of apoptosis-inhibitory agent, N-tosyl-L-phenylalanyl chloromethyl ketone against ischemia-induced hippocampal neuronal damage. J. Cereb. Blood Flow Metab. 18:1998;819-823.
12. Hara A., Yoshimi N., Hirose Y., Ino N., Tanaka T., Mori H. DNA fragmentation in granular cells of human cerebellum following global ischemia. Brain Res. 697:1995;247-250.
13. Hara A., Yoshimi N., Mori Y.H., Iwai T., Sakai N., Yamada H., Niwa M. Hypothermic prevention of nuclear DNA fragmentation in gerbil hippocampus following transient forebrain ischemia. Neurol. Res. 17:1995;461-464.
14. Hockenbery D. Defining apoptosis. Am. J. Pathol. 146:1995;16-19.
15. Hotz M.A., Gong J., Traganos F., Darzynkiewicz Z. Flow cytometric detection of apoptosis: comparison of the assays of in situ DNA degradation and chromatin changes. Cytometry. 15:1994;237-244.
16. Iwai T., Hara A., Niwa M., Nozaki M., Uematsu T., Sakai N., Yamada H. Temporal profile of nuclear DNA fragmentation in situ in gerbil hippocampus following transient forebrain ischemia. Brain Res. 671:1995;305-308.
17. Kass G.E., Eriksson J.E., Weis M., Orrenius S., Chow S.C. Chromatin condensation during apoptosis requires ATP. Biochem. J. 318:1996;749-752.
18. Kerr J.F., Winterford C.M., Harmon B.V. Apoptosis: Its significance in cancer and cancer therapy. Cancer. 73:1994;2013-2026.
19. Levee M.G., Dabrowska M.I., Lelli J.L. Jr., Hinshaw D.B. Actin polymerization and depolymerization during apoptosis in HL-60 cells. Am. J. Physiol. 271:1996;1981-1992.
20. Lind R.W. Angiotensin and the lamina terminalis: illustrations of a complex unity. Clin. Exp. Hypertens. 10:1988;79-105.
21. Lucassen P.J., Chung W.C., Vermeulen J.P., van Lookeren Campagne M., van Dierendonck J.H., Swaab D.F. Microwave-enhanced in situ end-labeling of fragmented DNA: parametric studies in relation to postmortem delay and fixation of rat and human brain. J. Histochem. Cytochem. 43:1995;1163-1171.
22. MacManus J.P., Buchan A.M., Hill I.E., Rasquinha I., Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164:1993;89-92.
23. Migheli A., Cavalla P., Marino S., Schiffer D. A study of apoptosis in normal and pathologic nervous tissue after in situ end-labeling of DNA strand breaks. J. Neuropathol. Exp. Neurol. 53:1994;606-616.
24. Mochizuki H., Mori H., Mizuno Y. Apoptosis in neurodegenerative disorders. J. Neural Transm. 50:1997;125-140.
25. Negoescu A., Lorimier P., Labat-Moleur F., Drouet C., Robert C., Guillermet C., Brambilla C., Brambilla E. In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. J. Histochem. Cytochem. 44:1996;959-968.
26. Nitatori T., Sato N., Waguri S., Karasawa Y., Araki H., Shibanai K., Kominami E., Uchiyama Y. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1995;1001-1011.
27. Niwa M., Hara A., Iwai T., Nakashima M., Yano H., Yoshimi N., Mori H., Uematsu T. Relationship between magnitude of hypothermia during ischemia and preventive effect against post-ischemic DNA fragmentation in the gerbil hippocampus. Brain Res. 794:1998;338-342.
28. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia: I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Rev. 20:1995;91-127.
29. Petito C.K., Roberts B. Effect of postmortem interval on in situ end-labeling of DNA oligonucleosomes. J. Neuropathol. Exp. Neurol. 54:1995;761-765.
30. Portera-Cailliau C., Hedreen J.C., Price D.L., Koliatsos V.E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15:1995;3775-3787.
31. Simonati A., Rosso T., Rizzuto N. DNA fragmentation in normal development of the human central nervous system: a morphological study during corticogenesis. Neuropathol. Appl. Neurobiol. 23:1997;203-211.
32. Toth I.E., Palkovits M. Viral labelling of synaptically connected neurons. Neurobiology. 5:1997;17-41.
33. White F.A., Keller-Peck C.R., Knudson C.M., Korsmeyer S.L., Snider W.D. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18:1998;1428-1439.
34. Whiteside G., Cougnon N., Hunt S.P., Munglani R. An improved method for detection of apoptosis in tissue sections and cell culture, using the TUNEL technique combined with Hoechst stain. Brain Res. Protocols. 2:1998;160-164.