Live fluorescence and transmission-through-dye microscopic study of actinomycin D-induced apoptosis and apoptotic volume decrease

Apoptosis

Volumn 18, Issue 4, 2013, Pages 521-532

  Kasim, Neda R ^a   Kuželová, Kateřina ^b   Holoubek, Aleš ^b   Model, Michael A ^a  

^a KENT STATE UNIVERSITY   (United States)

^b INSTITUTE OF HEMATOLOGY AND BLOOD TRANSFUSION   (Czech Republic)

Author keywords

Actinomycin D; Apoptotic volume decrease; Blebbing; Caspase 3; Caspase 7; Intracellular potassium; Intracellular sodium; Transmission through dye microscopy

Indexed keywords

CASPASE 3; CASPASE 7; DACTINOMYCIN;

APOPTOSIS; ARTICLE; CELL SHAPE; CELL STRUCTURE; CELL SWELLING; CELL VOLUME; CHROMATIN CONDENSATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE MICROSCOPY; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL;

APOPTOSIS; CALCIUM CHANNEL BLOCKERS; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CELL SIZE; CHROMATIN; DACTINOMYCIN; ENZYME ACTIVATION; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; PROTEASE INHIBITORS; PROTEIN SYNTHESIS INHIBITORS; SODIUM;

EID: 84876062889     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0804-z     Document Type: Article

References (74)

1. Kerr JF (1971) Shrinkage necrosis: a distinct mode of cellular death. J Pathol 105:13-20. doi: 10.1002/path.1711050103
2. Willingham MC (1999) Cytochemical methods for the detection of apoptosis. J Histochem Cytochem 47:1101-1110. doi: 10.1177/002215549904700901
3. Ziegler U, Groscurth P (2004) Morphological features of cell death. News Physiol Sci 19:124-128. doi: 10.1152/nips.01519.2004
4. Mashima T, Naito M, Tsuruo T (1999) Caspase-mediated cleavage of cytoskeletal actin plays a positive role in the process of morphological apoptosis. Oncogene 18:2423-2430. doi: 10.1038/sj.onc.1202558
5. Kothakota S, Azuma T, Reinhard C, Klippel A, Tang J, Chu K, McGarry TJ, Kirschner MW, Koths K, Kwiatkowski DJ, Williams LT (1997) Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278:294-298. doi: 10.1126/science.278.5336.294
6. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3:339-345. doi: 10.1038/35070009
7. Ndozangue-Touriguine O, Hamelin J, Bréard J (2008) Cytoskeleton and apoptosis. Biochem Pharmacol 76:11-18. doi: 10.1016/j.bcp.2008.03.016
8. Cotter TG, Lennon SV, Glynn JM, Green DR (1992) Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res 52:997-1005
9. Marushige Y, Marushige K (1998) Alterations in focal adhesion and cytoskeletal proteins during apoptosis. Anticancer Res 18:301-307
10. Wen L-P, Fahri JA, Troie S, Guan J-L, Orth K, Rosen GD (1997) Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem 272:26056-26061. doi: 10.1074/jbc.272.41.26056
11. Kim S, Kim DH, Shim SR, Kim W, Chun JS, Song WK (2003) Caspase-dependent cleavage of tensin induces disruption of actin cytoskeleton during apoptosis. Biochem Biophys Res Commun 303:37-45
12. McCarthy JV, Cotter TG (1997) Cell shrinkage and apoptosis: a role for potassium and sodium ion efflux. Cell Death Differ 4:756-770. doi: 10.1038/sj.cdd.4400296
13. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97:9487-9492. doi: 10.1073/pnas.140216197
14. 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. doi: 10.1021/la051837g
15. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S (2001) Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol 532:3-16. doi: 10.1111/j.1469-7793.2001.0003g.x
16. 2+ mobilization is a prerequisite to apoptosis in HeLa cells. Apoptosis 17:821-831. doi: 10.1007/s10495-012-0716-3
17. + efflux in the activation of apoptosis. J Biol Chem 272:32436-32442. doi: 10.1074/jbc.272.51.32436
18. Ernest NJ, Habela CW, Sontheimer H (2008) Cytoplasmic condensation is both necessary and sufficient to induce apoptotic cell death. J Cell Sci 121:290-297. doi: 10.1242/jcs.017343
19. Friis MB, Friborg CR, Schneider L, Nielsen MB, Lambert IH, Christensen ST, Hoffmann EK (2005) Cell shrinkage as a signal to apoptosis in NIH 3T3 fibroblasts. J Physiol 567:427-443. doi: 10.1113/jphysiol.2005.087130
20. Bortner CD, Cidlowski JA (2007) Cell shrinkage and monovalent cation fluxes: role in apoptosis. Arch Biochem Biophys 462:176-188. doi: 10.1016/j.abb.2007.01.020
21. + channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch 448:274-286. doi: 10.1007/s00424-004-1258-5
22. Yu SP (2003) Regulation and critical role of potassium homeostasis in apoptosis. Prog Neurobiol 70:363-386. doi: 10.1016/S0301-0082(03)00090-X
23. Hortelano S, Zeini M, Castrillo A, Alvarez AM, Boscá L (2002) Induction of apoptosis by nitric oxide in macrophages is independent of apoptotic volume decrease. Cell Death Differ 9:643-650. doi: 10.1038/sj.cdd.4401017
24. + influx is required for volume loss during programmed cell death. J Biol Chem 278:39176-39184. doi: 10.1074/jbc.M303516200
25. Yurinskaya V, Goryachaya T, Guzhova I, Moshkov A, Rozanov Y, Sakuta G, Shirokova A, Shumilina E, Vassilieva I, Lang F, Vereninov A (2005) Potassium and sodium balance in U937 cells during apoptosis with and without cell shrinkage. Cell Physiol Biochem 16:155-162. doi: 10.1159/000089841
26. Krumschnabel G, Maehr T, Nawaz M, Schwarzbaum PJ, Manzl C (2007) Staurosporine-induced cell death in salmonid cells: the role of apoptotic volume decrease, ion fluxes and MAP kinase signaling. Apoptosis 12:1755-1768. doi: 10.1007/s10495-007-0103-7
27. Wei L, Xiao AY, Jin C, Yang A, Lu ZY, Yu SP (2004) Effects of chloride and potassium channel blockers on apoptotic cell shrinkage and apoptosis in cortical neurons. Pflugers Arch 448:325-334. doi: 10.1007/s00424-004-1277-2
28. Platonova A, Koltsova SV, Hamet P, Grygorczyk R, Orlov SN (2012) Swelling rather than shrinkage precedes apoptosis in serum-deprived vascular smooth muscle cells. Apoptosis 17:429-438. doi: 10.1007/s10495-011-0694-x
29. Poulsen KA, Andersen EC, Hansen CF, Klausen TK, Hougaard C, Lambert IH, Hoffmann EK (2010) Deregulation of apoptotic volume decrease and ionic movements in multidrug-resistant tumor cells: role of chloride channels. Am J Physiol Cell Physiol 298:C14-C25. doi: 10.1152/ajpcell.00654.2008
30. Fiers W, Beyaert R, Declercq W, Vandenabeele P (1999) More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 18:7719-7730. doi: 10.1038/sj.onc.1203249
31. Silva MT (2010) Secondary necrosis: the natural outcome of the complete apoptotic program. FEBS Lett 584:4491-4499. doi: 10.1016/j.febslet.2010.10.046
32. 2+, and volume inside cultured adult rabbit cardiac myocytes during chemical hypoxia: a multiparameter digitized confocal microscopic study. Biophys J 66:942-952. doi: 10.1016/S0006-3495(94)80904-X
33. Lionetto MG, Giordano ME, Calisi A, Caricato R, Hoffmann E, Schettino T (2010) Role of BK channels in the apoptotic volume decrease in native eel intestinal cells. Cell Physiol Biochem 25:733-744. doi: 10.1159/000315093
34. Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J 38:244-259. doi: 10.1111/j.1365-313X.2004.02040.x
35. Boudreault F, Grygorczyk R (2004) Evaluation of rapid volume changes of substrate-adherent cells by conventional microscopy 3D imaging. J Microsc 215:302-312. doi: 10.1111/j.0022-2720.2004.01378.x
36. Platonova A, Koltsova S, Maksimov GV, Grygorczyk R, Orlov SN (2011) The death of ouabain-treated renal epithelial C11-MDCK cells is not mediated by swelling-induced plasma membrane rupture. J Membr Biol 241:145-154. doi: 10.1007/s00232-011-9371-9
37. Model MA (2012) Imaging the cell's third dimension. Microsc Today 20:32-37. doi: 10.1017/S1551929512000247
38. Kuželová K, Grebeňová D, Brodská B (2011) Dose-dependent effects of the caspase inhibitor Q-VD-OPh on different apoptosis-related processes. J Cell Biochem 112:3334-3342. doi: 10.1002/jcb.23263
39. Model MA, Khitrin AK, Blank JL (2008) Measurement of the absorption of concentrated dyes and their use for quantitative imaging of surface topography. J Microsc 231:156-167. doi: 10.1111/j.1365-2818.2008.02026.x
40. Gregg JL, McGuire KM, Focht DC, Model MA (2010) Measurement of the thickness and volume of adherent cells using transmission-through-dye microscopy. Pflugers Arch 460:1097-1104. doi: 10.1007/s00424-010-0869-2
41. Pelts M, Pandya SM, Oh CJ, Model MA (2011) Thickness profiling of formaldehyde-fixed cells by transmission-through-dye microscopy. Biotechniques 50:389-396
42. Lababidi SL, Pelts M, Moitra M, Leff LG, Model MA (2011) Measurement of bacterial volume by transmission-through-dye imaging. J Microbiol Methods 87:375-377. doi: 10.1016/j.mimet.2011.08.019
43. Kuzelová K, Grebenová D, Hrkal Z (2007) Labeling of apoptotic JURL-MK1 cells by fluorescent caspase-3 inhibitor FAM-DEVD-fmk occurs mainly at site(s) different from caspase-3 active site. Cytometry A 71:605-611. doi: 10.1002/cyto.a.20415
44. Goldstein MN, Slotnik IJ, Journey LJ (1960) In vitro studies with HeLa cell lines sensitive and resistant to actinomycin D. Ann N Y Acad Sci 89:474-483. doi: 10.1111/j.1749-6632.1960.tb20171.x
45. Clark AM, Love R, Studzinski GP, Ellem KA (1967) A correlated morphological and functional study of the effects of actinomycin D on HeLa cells. I. Effects on the nucleolar and cytoplasmic ribonucleoproteins. Exp Cell Res 45:106-119. doi: 10.1016/0014-4827(67)90116-4
46. Chou CC, Lam CY, Yung BY (1995) Intracellular ATP is required for actinomycin D-induced apoptotic cell death in HeLa cells. Cancer Lett 96:181-187. doi: 10.1016/0304-3835(95)03927-O
47. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2:156-162
48. Gao W, Pu Y, Luo KQ, Chang DC (2001) Temporal relationship between cytochrome c release and mitochondrial swelling during UV-induced apoptosis in living HeLa cells. J Cell Sci 114:2855-2862
49. Fraschini A, Bottone MG, Scovassi AI, Denegri M, Risueño MC, Testillano PS, Martin TE, Biggiogera M, Pellicciari C (2005) Changes in extranucleolar transcription during actinomycin D-induced apoptosis. Histol Histopathol 20:107-117
50. + in HeLa cells. FEBS Lett 424:221-224. doi: 10.1016/S0014-5793(98) 00172-0
51. Maeno E, Takahashi N, Okada Y (2006) Dysfunction of regulatory volume increase is a key component of apoptosis. FEBS Lett 580:6513-6517. doi: 10.1016/j.febslet.2006.10.074
52. Hasegawa Y, Shimizu T, Takahashi N, Okada Y (2012) The apoptotic volume decrease is an upstream event of MAP kinase activation during staurosporine-induced apoptosis in HeLa cells. Int J Mol Sci 13:9363-9379. doi: 10.3390/ijms13079363
53. Barrett KL, Willingham JM, Garvin AJ, Willingham MC (2001) Advances in cytochemical methods for detection of apoptosis. J Histochem Cytochem 49:821-832. doi: 10.1177/002215540104900703
54. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Castedo M, Cidlowski JA, Ciechanover A, Cohen GM, De Laurenzi V, De Maria R, Deshmukh M, Dynlacht BD, El-Deiry WS, Flavell RA, Fulda S, Garrido C, Golstein P, Gougeon ML, Green DR, Gronemeyer H, Hajnóczky G, Hardwick JM, Hengartner MO, Ichijo H, Jäättelä M, Kepp O, Kimchi A, Klionsky DJ, Knight RA, Kornbluth S, Kumar S, Levine B, Lipton SA, Lugli E, Madeo F, Malomi W, Marine JC, Martin SJ, Medema JP, Mehlen P, Melino G, Moll UM, Morselli E, Nagata S, Nicholson DW, Nicotera P, Nuñez G, Oren M, Penninger J, Pervaiz S, Peter ME, Piacentini M, Prehn JH, Puthalakath H, Rabinovich GA, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Scorrano L, Simon HU, Steller H, Tschopp J, Tsujimoto Y, Vandenabeele P, Vitale I, Vousden KH, Youle RJ, Yuan J, Zhivotovsky B, Kroemer G (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16:1093-1107
55. Gómez-Angelats M, Cidlowski JA (2002) Cell volume and ion changes during apoptotic cell death. Adv Cancer Res 85:175-201. doi: 10.1016/S0065-230X(02)85006-0
56. Formigli L, Papucci L, Tani A, Schiavone N, Tempestini A, Orlandini GE, Capaccioli S, Orlandini SZ (2000) Aponecrosis: morphological and biochemical exploration of a syncretic process of cell death sharing apoptosis and necrosis. J Cell Physiol 182:41-49. doi: 10.1002/(SICI)1097-4652(200001)182:1<41:AID- JCP5>3.0.CO;2-7
57. Yu SP (2003) Na +, K + -ATPase: the new face of an old player in pathogenesis and apoptotic/hybrid cell death. Biochem Pharmacol 66:1601-1609. doi: 10.1016/S0006-2952(03)00531-8
58. Bock J, Szabó I, Jekle A, Gulbins E (2002) Actinomycin D-induced apoptosis involves the potassium channel Kv1.3. Biochem Biophys Res Commun 295:526-531. doi: 10.1016/S0006-291X(02)00695-2
59. + ratio blocks apoptosis in vascular smooth muscle at a site upstream of caspase-3. J Biol Chem 274:16545-16552. doi: 10.1074/jbc.274.23.16545
60. +-ATPase please stand up? Acta Physiol (Oxf) 187:205-215. doi: 10.1111/j.1748-1716.2006. 01562.x
61. + pump suppression not cause cell swelling? J Physiol 589:2197-2211. doi: 10.1113/jphysiol.2011.207571
62. Platonova A, Koltsova S, Maksimov GV, Grygorczyk R, Orlov SN (2011) The death of ouabain-treated renal epithelial C11-MDCK cells is not mediated by swelling-induced plasma membrane rupture. J Membr Biol 241:145-514. doi: 10.1007/s00232-011-9371-9
63. Fels J, Orlov SN, Grygorczyk R (2009) The hydrogel nature of mammalian cytoplasm contributes to osmosensing and extracellular pH sensing. Biophys J 96:4276-4285. doi: 10.1016/j.bpj.2009.02.038
64. Crawford ED, Wells JA (2011) Caspase substrates and cellular remodeling. Annu Rev Biochem 80:1055-1087. doi: 10.1146/annurev-biochem-061809-121639
65. Lang F, Madlung J, Uhlemann AC, Risler T, Gulbins E (1998) Cellular taurine release triggered by stimulation of the Fas(CD95) receptor in Jurkat lymphocytes. Pflugers Arch 436:377-383. doi: 10.1007/s004240050646
66. Sreedhar AS, Csermely P (2004) Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy: a comprehensive review. Pharmacol Ther 101:227-257
67. Lew VL, Bookchin RM (2005) Ion transport pathology in the mechanism of sickle cell dehydration. Physiol Rev 85:179-200. doi: 10.1152/physrev.00052.2003
68. Spagnoli C, Beyder A, Besch S, Sachs F (2008) Atomic force microscopy analysis of cell volume regulation. Phys Rev E Stat Nonlin Soft Matter Phys 78:031916
69. Domnina LV, Ivanova OY, Cherniak BV, Skulachev VP, Vasiliev JM (2002) Effects of the inhibitors of dynamics of cytoskeletal structures on the development of apoptosis induced by the tumor necrosis factor. Biochemistry (Mosc) 67:737-746
70. Brown TL, Patil S, Cianci CD, Morrow JS, Howe PH (1999) Transforming growth factor β induces caspase 3-independent cleavage of αII-spectrin (α-fodrin) coincident with apoptosis. J Biol Chem 274:23256-23262. doi: 10.1074/jbc.274.33.23256
71. Cui Q, Yu JH, Wu JN, Tashiro S, Onodera S, Minami M, Ikejima T (2007) P53-mediated cell cycle arrest and apoptosis through a caspase-3- independent, but caspase-9-dependent pathway in oridonin-treated MCF-7 human breast cancer cells. Acta Pharmacol Sin 28:1057-1066. doi: 10.1111/j.1745-7254.2007.00588.x
72. Higuchi M, Honda T, Proske RJ, Yeh ET (1998) Regulation of reactive oxygen species-induced apoptosis and necrosis by caspase 3-like proteases. Oncogene 17:2753-2760. doi: 10.1038/sj.onc.1202211
73. Sebbagh M, Hamelin J, Bertoglio J, Solary E, Bréard J (2005) Direct cleavage of ROCK II by granzyme B induces target cell membrane blebbing in a caspase-independent manner. J Exp Med 201:465-471. doi: 10.1084/jem.20031877
74. Harwood SM, Yaqoob MM, Allen DA (2005) Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann Clin Biochem 42:415-431. doi: 10.1258/000456305774538238