Apoptotic DNA fragmentation can be revealed in situ: An ultrastructural approach

Microscopy Research and Technique

Volumn 72, Issue 12, 2009, Pages 913-923

  Burattini, Sabrina ^a   Ferri, Paola ^a   Battistelli, Michela ^b   D'Emilio, Alessandra ^a   Biagiotti, Laura ^a   Sestili, Piero ^a   Rocchi, Marco B L ^a   Falcieri, Elisabetta ^a,c  

^a UNIVERSITY OF URBINO   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c CNR   (Italy)

Author keywords

Electron microscopy; TUNEL; U937 and Molt 4; UVB and staurosporine

Indexed keywords

CELL DEATH; CHROMOSOMES; CONDENSATION; DNA; ELECTRON MICROSCOPES; GOLD;

APOPTOTIC; CHROMATIN CONDENSATION; DNA CLEAVAGE; DNA FRAGMENTATION; GOLD PARTICLES; PARTICLE DENSITIES; STAUROSPORINES; TUNEL; U937 AND MOLT-4; UVB AND STAUROSPORINE;

ELECTRON MICROSCOPY;

DNA FRAGMENT; GOLD DERIVATIVE; STAUROSPORINE;

APOPTOSIS; ARTICLE; CELL STRAIN U937; CHROMATIN CONDENSATION; CONTROLLED STUDY; DENSITY; DNA CLEAVAGE; DNA FRAGMENTATION; DNA STRAND BREAKAGE; ELECTRON MICROSCOPY; ELECTROPHORESIS; HUMAN; HUMAN CELL; NICK END LABELING; PRIORITY JOURNAL; ULTRASTRUCTURE; ULTRAVIOLET B RADIATION;

EID: 72249093940     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.20735     Document Type: Article

References (62)

1. Andreev IO, Solovyan VT, Spiridonova KV, Kunakh VA. 2005. Changes in a pattern of HMW-DNA fragmentation accompany differentiation and ageing of plant cells. BMC Plant Biol 5 (Suppl 1):S2.
2. Ansari B, Coates PJ, Greenstein BD, Hall PA. 1993. In situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol 170:1-8.
3. Arends MJ, Morris RG, Wyllie AH. 1990. Apoptosis. The role of the endonuclease. Am J Pathol 136:593-608.
4. Bao Y, Shen X. 2007. Chromatin remodeling in DNA double-strand break repair. Curr Opin Genet Dev 17:126-131. (Pubitemid 46551721)
5. Begemann M, Kashimawo SA, Heitjan DF, Schiff PB, Bruce JN, Weinstein IB. 1998. Treatment of human glioblastoma cells with the staurosporine derivative CGP 41251 inhibits CDC2 and CDK2 kinase activity and increases radiation sensitivity. Anticancer Res 18:2275-2282. (Pubitemid 28386507)
6. Brown DG, Sun XM, Cohen GM. 1993. Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J Biol Chem 268:3037-3039. (Pubitemid 23070921)
7. Burattini S, Luchetti F, Battistelli M, Della Felice M, Papa S, Piersanti G, Tarzia G, Falcieri E. 2003. 5-(2-Ethyl-phenyl)-3-(3- methoxy-phenyl)-1H-[1, 2,4]triazole (DL-111-IT) and related compounds induce apoptotic patterns in cultures of human tumor cell lines. J Biol Regul Homeost Agents 17:348-357.
8. Burattini S, Ferri P, Battistelli M, Curci R, Luchetti F, Falcieri E. 2004. C2C12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization. Eur J Histochem 48:223-233.
9. Caricchio R, Reap EA, Cohen PL. 1998. Fas/Fas ligand interactions are involved in ultraviolet-B-induced human lymphocyte apoptosis. J Immunol 161:241-251. (Pubitemid 28285529)
10. Cohen GM, Sun XM, Fearnhead H, MacFarlane M, Brown DG, Snowden RT, Dinsdale D. 1994. Formation of large molecular weight fragments of DNA is a key committed step of apoptosis in thymocytes. J Immunol 153:507-516. (Pubitemid 24206280)
11. Collins RJ, Harmon BV, Gobé GC, Kerr JF. 1992. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int J Radiat Biol 61:451-453.
12. Counis MF, Torriglia A. 2000. DNases and apoptosis. Biochem Cell Biol 78:405-414.
13. Czene S, Testa E, Nygren J, Belyaev I, Harms-Ringdahl M. 2002. DNA fragmentation and morphological changes in apoptotic human lymphocytes. Biochem Biophys Res Commun 294:872-878. (Pubitemid 34687197)
14. Falcieri E, Martelli AM, Bareggi R, Cataldi A, Cocco L. 1993. The protein kinase inhibitor staurosporine induces morphological changes typical of apoptosis in MOLT-4 cells without concomitant DNA fragmentation. Biochem Biophys Res Commun 193:19-25. (Pubitemid 23199907)
15. Formichi P, Radi E, Battisti C, Tarquini E, Leonini A, Di Stefano A, Federico A. 2006. Human fibroblasts undergo oxidative stress-induced apoptosis without internucleosomal DNA fragmentation. J Cell Physiol 208:289-297. (Pubitemid 43993419)
16. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
17. Goping G, Wood KA, Sei Y, Pollard HB. 1999. Detection of fragmented DNA in apoptotic cells embedded in LR white: A combined histochemical (LM) and ultrastructural (EM) study. J Histochem Cytochem 47:561-568. (Pubitemid 29162855)
18. Hara A, Niwa M, Kumada M, Kitaori N, Yamamoto T, Kozawa O, Mori H. 2004. Fragmented DNA transport in dendrites of retinal neurons during apoptotic cell death. Brain Res 1007:183-187. (Pubitemid 38520187)
19. Hu Y, Yao J, Liu X, Fu H, Ye K. 2005. Akt phosphorylate acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J 24:3543-3554. (Pubitemid 41509362)
20. Huang P, Robertson LE, Wright S, Plunkett W. 1995. High molecular weight DNA fragmentation: a critical event in nucleoside analogue-induced apoptosis in leukemia cells. Clin Cancer Res 1:1005-1013.
21. Iguki K, Hirano K, Ishida R. 2002. Activation of caspase-3, proteolytic cleavage of DFF and no oligonucleosomal DNA fragmentation in apoptotic Molt-4 cells. J Biochem 131:469-475. (Pubitemid 34292839)
22. Ishida-Yamamoto A, Yamauchi T, Tanaka H, Nakane H, Takahashi H, Iizuka H.J. 1999. Electron microscopic in situ DNA nick end-labeling in combination with immunoelectron microscopy. Histochem Cytochem 47:711-717.
23. Ito Y, Shibata MA, Kusakabe K, Otsuki Y. 2006. Method of specific detection of apoptosis using formamide-induced DNA denaturation assay. J Histochem Cytochem 54:683-692. (Pubitemid 43736891)
24. Jackson SP. 2001. Detecting, signalling and repairing DNA double-strand breaks. Biochem Soc Trans 29:655-661. (Pubitemid 33131755)
25. Johnson VL, Ko SC, Holmstrom TH, Eriksson JE, Chow SC. 2000. Effector caspases are dispensable for the early nuclear morphological changes during chemical-induced apoptosis. J Cell Sci 113 (Pt 17):2941-2953.
26. Joselin AP, Schulze-Osthoff K, Schwerk C. 2006. Loss of Acinus inhibits oligonucleosomal DNA fragmentation but not chromatin condensation during apoptosis. J Biol Chem 281:12475-12484. (Pubitemid 43855334)
27. Kawashima K, Doi H, Ito Y, Shibata MA, Yoshinaka R, Otsuki Y. 2004. Evaluation of cell death and proliferation in psoriatic epidermis. J Dermatol Sci 35:207-214. (Pubitemid 39295695)
28. Kelly KJ, Sandoval RM, Dunn KW, Molitoris BA, Dagher PC. 2003. A novel method to determine specificity and sensitivity of the TUNEL reaction in the quantitation of apoptosis. Am J Physiol Cell Physiol 284:C1309-C1318.
29. Kumagai K, Otsuki Y, Ito Y, Shibata MA, Abe H, Ueki M. 2001. Apoptosis in the normal human amnion at term, independent of Bcl-2 regulation and onset of labour. Mol Hum Reprod 7:681-689. (Pubitemid 32633418)
30. Kuribayashi N, Sakagami H, Iida M, Takeda M. 1996. Chromatin structure and endonuclease sensitivity in human leukemic cell lines. Anticancer Res 16:1225-1230. (Pubitemid 26229792)
31. Lindahl T, Satoh MS, Poirier GG, Klungland A. 1995. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20:405-411.
32. Lossi L, Mioletti S, Merighi A. 2002a. Synapse-independent and synapse- dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages. Neuroscience 112:509-523. (Pubitemid 34634146)
33. Lossi L, Mioletti S, Aimar P, Bruno R, Merighi A. 2002b. In vivo analysis of cell proliferation and apoptosis in the CNS. In A. Merighi, G. Carmignoto. Cellular and molecular methods in neuroscience research. (pp.303). New York: Springer-Verlag (United States).
34. Luchetti F, Gregorini A, Papa S, Burattini S, Canonico B, Valentini M, Falcieri E. 1998. The K562 chronic myeloid leukemia cell line undergoes apoptosis in response to interferon-alpha. Haematologica 83:974-980. (Pubitemid 29039464)
35. Luchetti F, Burattini S, Ferri P, Papa S, Falcieri E. 2002. Actin involvement in apoptotic chromatin changes of hemopoietic cells undergoing hyperthermia. Apoptosis 7:143-152. (Pubitemid 34273129)
36. Luchetti F, Mannello F, Canonico B, Battistelli M, Burattini S, Falcieri E, Papa S. 2004. Integrin and cytoskeleton behaviour in human neuroblastoma cells during hyperthermia-related apoptosis. Apoptosis 9:635-648. (Pubitemid 39158640)
37. Luchetti F, Canonico B, Curci R, Battistelli M, Mannello F, Papa S, Tarzia G, Falcieri E. 2006. Melatonin prevents apoptosis induced by UV-B treatment in U937 cell line. J Pineal Res 40:158-167.
38. Mariani AR, Columbaro M, Zauli G, Zamai L, Luchetti F, Gobbi P, Ghibellini D, Falcieri E, Vitale M. 1999. Lineage-related susceptibility of human hemopoietic cell lines to apoptosis. Anat Rec 254:1-6. (Pubitemid 29024774)
39. Marini M, Musiani D, Sestili P, Cantoni O. 1996. Apoptosis of human lymphocytes in the absence or presence of internucleosomal DNA cleavage. Biochem Biophys Res Commun 229:910-915. (Pubitemid 27035816)
40. Nagata S. 2000. Apoptotic DNA fragmentation. Exp Cell Res 256:12-18.
41. Nakamura K, Ito Y, Matsumoto K, Daikoku E, Kiyokane K, Otsuki Y. 1999. The relationship between apoptosis and keratinisation in human epidermis. Acta Histochem Cytochem 32:77-83. (Pubitemid 29285252)
42. Oberhammer F, Wilson JW, Dive C, Morris ID, Hickman JA, Wakeling AE, Walker PR, Sikorska M. 1993. Apoptotic death in epithelial cells: cleavage of DNA to 300 and 50 kbp fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 12:3679-3684. (Pubitemid 23256455)
43. Otsuki Y. 2004. Tissue specificity of apoptotic signal transduction. Med Electron Microsc 37:163-169. (Pubitemid 40576034)
44. Placzek M, Przybilla B, Kerkmann U, Gaube S, Gilbertz KP. 2007. Effect of ultraviolet (UV) A, UVB or ionizing radiation on the cell cycle of human melanoma cells. Br J Dermatol 156:843-847. (Pubitemid 46642835)
45. Renò F, Burattini S, Rossi S, Luchetti F, Columbaro M, Santi S, Papa S, Falcieri E. 1998. Phospholipid rearrangement of apoptotic membrane does not depend on nuclear activity. Histochem Cell Biol 110:467-476. (Pubitemid 28480279)
46. Sakahira H, Enari M, Ohsawa Y, Uchiyama Y, Nagata S. 1999. Apoptotic nuclear morphological change without DNA fragmentation. Curr Biol 9:543-546. (Pubitemid 29257111)
47. Samejima K, Tone S, Earnshaw WC. 2001. CAD/DFF40 nuclease is dispensable for high molecular weight DNA cleavage and stage I chromatin condensation in apoptosis. J Biol Chem 276:45427-45432. (Pubitemid 37391341)
48. Sestili P, Cattabeni F, Cantoni O. 1996. Direct excision of 50 kb pair DNA fragments from megabase-sized fragments produced during apoptotic cleavage of genomic DNA. FEBS Lett 396:337-342. (Pubitemid 26377852)
49. Sestili P, Martinelli C, Bravi G, Piccoli G, Curci R, Battistelli M, Falcieri E, Agostini D, Gioacchini AM, Stocchi V. 2006. Creatine supplementation affords cytoprotection in oxidatively injured cultured mammalian cells via direct antioxidant activity. Free Radic Biol Med 40:837-849. (Pubitemid 43327318)
50. Sit KH, Yin L, Paramanantham R. 1997. Apoptotic condensations in M-phase cells. Anat Rec 248:149-158.
51. Solov'yan VT, Andreev IO, Kolotova TY, Pogribniy PV, Tarnavsky DT, Kunakh VA. 1997. The cleavage of nuclear DNA into high molecular weight DNA fragments occurs not only during apoptosis but also accompanies changes in functional activity of the nonapoptotic cells. Exp Cell Res 235:130-137.
52. Su TT. 2006. Cellular responses to DNA damage: One signal, multiple choices. Annu Rev Genet 40:187-208. (Pubitemid 44956784)
53. Takahashi H, Komatsu N, Ibe M, Ishida-Yamamoto A, Hashimoto Y, Iizuka H. 2007. Cystatin A suppresses ultraviolet B-induced apoptosis of keratinocytes. J Dermatol Sci 46:179-187. (Pubitemid 46601839)
54. Thiry M. 1991. In situ nick translation at the electron microscopic level: a tool for studying the location of DNAse I-sensitive regions within the cell. J Histochem Cytochem 39:871-874.
55. Thiry M. 1992. Highly sensitive immunodetection of DNA on sections with exogenous terminal deoxynucleotidyl transferase and non-isotopic nucleotide analogues. J Histochem Cytochem 40:411-419.
56. Tong L, Chen Z, De Paiva CS, Beuerman R, Li DQ, Pflugfelder SC. 2006. Transglutaminase participates in UVB-induced cell death pathways in human corneal epithelial cells. Invest Ophthalmol Vis Sci 47:4295-4301. (Pubitemid 46579351)
57. Vitale M, Zamai L, Falcieri E, Zauli G, Gobbi P, Santi S, Cinti C, Weber G. 1997. IMP dehydrogenase inhibitor, tiazofurin, induces apoptosis in K562 human erythroleukemia cells. Cytometry 30:61-66.
58. Wyllie AH. 1987. Apoptosis: cell death in tissue regulation. J Pathol 153:313-316. (Pubitemid 18008327)
59. Wyllie AH, Kerr JF, Currie AR. 1980. Cell death: The significance of apoptosis. Int Rev Cytol 68:251-306. Review.
60. Yanagisawa-Shiota F, Sakagami H, Kuribayashi N, Iida M, Sakagami T, Takeda M. 1995. Endonuclease activity and induction of DNA fragmentation in human myelogenous leukemic cell lines. Anticancer Res 15:259-265.
61. Yoshida A, Pommier Y, Ueda T. 2006. Endonuclease activation and chromosomal DNA fragmentation during apoptosis in leukemia cells. Int J Hematol 84:31-37.
62. Zamai L, Burattini S, Luchetti F, Canonico B, Ferri P, Melloni E, Gonelli A, Guidotti L, Papa S, Falcieri E. 2004. In vitro apoptotic cell death during erythroid differentiation. Apoptosis 9:235-246.