zbMATH — the first resource for mathematics

Nuclear apoptotic volume decrease in individual cells: confocal microscopy imaging and kinetic modeling. (English) Zbl 1406.92341
Summary: The dynamics of nuclear morphology changes during apoptosis remains poorly investigated and understood. Using 3D time-lapse confocal microscopy we performed a study of early-stage apoptotic nuclear morphological changes induced by etoposide in single living HepG2 cells. These observations provide a definitive evidence that nuclear apoptotic volume decrease (AVD) is occurring simultaneously with peripheral chromatin condensation (so called “apoptotic ring”). In order to describe quantitatively the dynamics of nuclear morphological changes in the early stage of apoptosis we suggest a general molecular kinetic model, which fits well the obtained experimental data in our study. Results of this work may clarify molecular mechanisms of nuclear morphology changes during apoptosis.
92C55 Biomedical imaging and signal processing
92C45 Kinetics in biochemical problems (pharmacokinetics, enzyme kinetics, etc.)
35Q92 PDEs in connection with biology, chemistry and other natural sciences
Full Text: DOI
[1] Allera, C.; Lazzarini, G.; Patrone, E.; Alberti, I.; Barboro, P.; Sanna, P.; Melchiori, A.; Parodi, S.; Balbi, C., The condensation of chromatin in apoptotic thymocytes shows a specific structural change, J. Biol. Chem., 272, 10817-10822, (1997)
[2] Artus, C.; Boujrad, H.; Bouharrour, A.; Brunelle, M.-N.; Hoos, S.; Yuste, V. J.; Lenormand, P.; Rousselle, J.-C.; Namane, A.; England, P.; Lorenzo, H. K.; Susin, S. A., AIF promotes chromatinolysis and caspaseindependent programmed necrosis by interacting with histone H2AX, EMBO J, 29, 1585-1599, (2010)
[3] Athirasala, A.; Hirsch, N.; Buxboim, A., Nuclear mechanotransduction: sensing the force from within, Curr. Opin. Cell Biol., 46, 119-127, (2017)
[4] Baritaud, M.; Boujrad, H.; Lorenzo, H. K.; Krantic, S.; Susin, S. A., Histone H2AX: the missing link in AIF-mediated caspase-independent programmed necrosis, Cell Cycle, 9, 3186-3193, (2010)
[5] Bhola, P. D.; Mattheyses, A. L.; Simon, S. M., Spatial and temporal dynamics of mitochondrial membrane permeability waves during apoptosis, Biophys. J., 97, 2222-2231, (2009)
[6] Candé, C.; Vahsen, N.; Garrido, C.; Kroemer, G., Apoptosis-inducing factor (AIF): caspase-independent after all, Cell Death Differ, 11, 591-595, (2004)
[7] Candé, C.; Cohen, I.; Daugas, E.; Ravagnan, L.; Larochette, N.; Zamzami, N.; Kroemer, G., Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria, Biochimie, 84, 215-222, (2002)
[8] Dahl, K. N.; Kahn, S. M.; Wilson, K. L.; Discher, D. E., The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber, J. Cell Sci., 117, 4779-4786, (2004)
[9] Gong, M.; Hay, S.; Marshall, K. R.; Munro, A. W.; Scrutton, N. S., DNA binding suppresses human AIF-M2 activity and provides a connection between redox chemistry, reactive oxygen species, and apoptosis, J. Biol. Chem., 282, 30331-30340, (2007)
[10] Han, W.; Shi, X.; Nuttall, A. L., AIF and endog translocation in noise exposure induced hair cell death, Hearing Res., 211, 85-95, (2006)
[11] Hangen, E.; Blomgren, K.; Bénit, P.; Kroemer, G.; Modjtahedi, N., Life with or without AIF, Trends Biochem. Sci, 35, 278-287, (2010)
[12] Hangen, E.; raud, O. F.; Lachkar, S.; Mou, H.; Doti, N.; Fimia, G. M.; Lam, N.; Zhu, C.; Godin, I.; Muller, K.; Chatzi, A.; Nuebel, E.; Ciccosanti, F.; Flamant, S.; nit, P. B.; Perfettini, J.-L.; Sauvat, A.; Bennaceur-Griscelli, A.; Roux, K. S.-L.; Gonin, P.; Tokatlidis, K.; Rustin, P.; Piacentini, M.; Ruvo, M.; Blomgren, K.; Kroemer, G.; Modjtahedi, N., Interaction between AIF and CHCHD4 regulates respiratory chain biogenesis, Mol. Cell, 58, 1001-1014, (2015)
[13] Hendzel, M. J.; Nishioka, W. K.; Raymond, Y.; Allis, C. D.; Bazett-Jones, D. P.; Th’ng, J. P.H., Chromatin condensation is not associated with apoptosis, J. Biol. Chem., 273, 24470-24478, (1998)
[14] Ho, T.-C.; Yang, Y.-C.; Cheng, H.-C.; Wu, A.-C.; Chen, S.-L.; Chen, H.-K.; Tsao, Y.-P., Activation of mitogen-activated protein kinases is essential for hydrogen peroxide -induced apoptosis in retinal pigment epithelial cells, Apoptosis, 11, 1899-1908, (2006)
[15] Javierre, E.; Vuik, C.; Vermolen, F. J.; Zwaag, S.v.d., A comparison of numerical models for one-dimensional Stefan problems, J. Comp. Appl. Math., 192, 445-459, (2006) · Zbl 1092.65072
[16] Jones, D. R.; Perttunen, C. D.; Stuckman, B. E., Lipschitzian optimization without the Lipschitz constant, J. Optim. Theory Appl., 79, 157-181, (1993) · Zbl 0796.49032
[17] Joza, N.; Pospisilik, J. A.; Hangen, E.; Hanada, T.; Modjtahedi, N.; Penninger, J. M.; Kroemera, G., AIF: not just an apoptosis-inducing factor, Ann. N.Y. Acad. Sci., 1171, 2-11, (2009)
[18] Kerr, J. F.R.; Wyllie, A. H.; Currie, A. R., Apoptosis: A basic biological phenomenon with wideranging implications in tissue kinetics, Br. J. Cancer, 26, 239-257, (1972)
[19] Kihlmark, M.; Imreh, G.; Hallberg, E., Sequential degradation of proteins from the nuclear envelope during apoptosis, J. Cell Sci., 114, 3643-3653, (2001)
[20] Lafarge, T.; Pateiro-López, B.; Possolo, A.; Dunkers, J. P., R implementation of a polyhedral approximation to a 3D set of points using the α-shape, J. Stat. Softw., 56, 1-19, (2014)
[21] Li, L. Y.; Luo, X.; Wang, X., Endonuclease G is an apoptotic dnase when released from mitochondria, Nature, 412, 95-99, (2001)
[22] Loo, G.v.; Saelens, X.; Gurp, M.v.; MacFarlane, M.; Martin, S. J.; Vandenabeele, P., The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet, Cell Death Differ., 9, 1031-1042, (2002)
[23] Ma, J.; Goryaynov, A.; Sarma, A.; Yang, W., Self-regulated viscous channel in the nuclear pore complex, PNAS, 109, 7326-7331, (2012)
[24] Martelli, A. M.; Zweyer, M.; Ochs, R. L.; Tazzari, P. L.; Tabellini, G.; Narducci, P.; Bortul, R., Nuclear apoptotic changes: an overview, J. Cell. Biochem., 82, 634-646, (2001)
[25] Maté, M. J.; Ortiz-Lombardía, M.; Boitel, B.; Haouz, A.; Tello, D.; Susin, S. A.; Penninger, J.; Kroemer, G.; Alzari, P. M., The crystal structure of the mouse apoptosis-inducing factor AIF, Nat. Struct. Biol., 9, 442-446, (2002)
[26] Meirmanov, A. M., The Stefan problem, (1992), Walter de Gruyter New York
[27] Mora-Bermudez, F.; Ellenberg, J., Measuring structural dynamics of chromosomes in living cells by fluorescence microscopy, Methods, 41, 158-167, (2007)
[28] Oberhammer, F.; Wilson, J. W.; Dive, C.; Morris, I. D.; Hickman, J. A.; Wakeling, A. E.; Walker, P. R.; Sikorska, M., Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation, EMBO J, 12, 3679-3684, (1993)
[29] Orlova, D. Y.; Bártová, E.; Maltsev, V. P.; Kozubek, S.; Chernyshev, A. V., A nonfitting method using a spatial sine window transform for inhomogeneous effective diffusion measurements by FRAP, Biophys. J., 100, 507-516, (2011)
[30] Pantic, I.; Harhaji-Trajkovic, L.; Pantovic, A.; Milosevic, N.; Trajkovic, V., Changes infractal dimension and lacunarity as early markers of UV-induced apoptosis, J. Theor. Biol., 303, 87-92, (2012)
[31] Patterson, G. H.; Knobel, S. M.; Sharif, W. D.; Kain, S. R.; Piston, D. W., Use of the Green fluorescent protein and its mutants in quantitative fluorescence microscopy, Biophys. J., 73, 2782-2790, (1997)
[32] Pawley, J., Handbook of biological confocal microscopy, (2010), Springer Science & Business Media
[33] Robertson, J. D.; Orrenius, S.; Zhivotovsky, B., Review: nuclear events in apoptosis, J. Struct. Biol., 129, 346-358, (2000)
[34] Rubinšteĭn, L. I., Translations of mathematical monographs the Stefan problem, Am. Math. Soc., 27, 419, (2000)
[35] Samejima, K.; Earnshaw, W. C., Trashing the genome: the role of nucleases during apoptosis, Nat. Rev. Mol. Cell Biol., 6, 677-688, (2005)
[36] Saraste, A.; Pulkki, K., Morphologic and biochemical hallmarks of apoptosis, Cardiovasc. Res., 45, 528-537, (2000)
[37] Scovassi, A. I.; Soldani, C.; Veneroni, P.; Bottone, M. G.; Pellicciarib, C., Changes of mitochondria and relocation of the apoptosis inducing factor during apoptosis, Ann. N.Y. Acad. Sci., 1171, 12-17, (2009)
[38] Sesso, A.; Belizario, J. E.; Marques, M. M.; Higuchi, M. L.; Schumacher, R. I.; Colquhoun, A.; Ito, E.; Kawakami, J., Mitochondrial swelling and incipient outer membrane rupture in preapoptotic and apoptotic cells, Anat. Rec., 295, 1647-1659, (2012)
[39] Sevrioukova, I. F., Apoptosis-inducing factor: structure, function, and redox regulation, Antioxid Redox Signal, 14, 2545-2579, (2011)
[40] Solier, S.; Pommier, Y., The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases, Cell Cycle, 8, 1853-1859, (2009)
[41] Solier, S.; Pommier, Y., The nuclear γ-H2AX apoptotic ring: implications for cancers and autoimmune diseases, Cell. Mol. Life Sci., 71, 2289-2297, (2014)
[42] Stewart, M., Molecular mechanism of the nuclear protein import cycle, Nat. Rev. Mol. Cell Biol., 8, 195-208, (2007)
[43] Sun, M. G.; Williams, J.; Munoz-Pinedo, C.; Perkins, G. A.; Brown, J. M.; Ellisman, M. H.; Green, D. R.; Frey, T. G., Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis, Nat. Cell Biol., 9, 1057-1065, (2007)
[44] Sun, Y.; Gao, W.; Zhao, Y.; Cao, W.; Liu, Z.; Cui, G.; Tong, L.; Lei, F.; Tang, B., Visualization and inhibition of mitochondria-nuclear translocation of apoptosis inducing factor by a graphene oxide-DNA nanosensor, Anal. Chem., 89, 4642-4647, (2017)
[45] Susin, S. A.; Daugas, E.; Ravagnan, L.; Samejima, K.; Zamzami, N.; Loeffler, M.; Costantini, P.; Ferri, K. F.; Irinopoulou, T.; Prévost, M.-C.; Brothers, G.; Mak, T. W.; Penninger, J.; Earnshaw, W. C.; Kroemer, G., Two distinct pathways leading to nuclear apoptosis, J. Exp. Med., 192, 571-580, (2000)
[46] Susin, S. A.; Lorenzo, H. K.; Zamzami, N.; Marzo, I.; Snow, B. E.; Brothers, G. M.; Mangion, J.; Jacotot, E.; Costantini, P.; Loeffler, M.; Larochette, N.; Goodlett, D. R.; Aebersold, R.; Siderovski, D. P.; Penninger, J. M.; Kroemer, G., Molecular characterization of mitochondrial apoptosis-inducing factor, Nature, 397, 441-446, (1999)
[47] Tone, S.; Sugimoto, K.; Tanda, K.; Suda, T.; Uehira, K.; Kanouchi, H.; Samejima, K.; Minatogawa, Y.; Earnshaw, W. C., Three distinct stages of apoptotic nuclear condensation revealed by time-lapse imaging, biochemical and electron microscopy analysis of cell-free apoptosis, Exp. Cell Res., 313, 3635-3644, (2007)
[48] Vahsen, N.; Cande, C.; Dupaigne, P.; Giordanetto, F.; Kroemer, R. T.; Herker, E.; Scholz, S.; Modjtahedi, N.; Madeo, F.; Cam, E. L.; Kroemer, G., Physical interaction of apoptosis-inducing factor with DNA and RNA, Oncogene, 25, 1763-1774, (2006)
[49] Versaevel, M.; Grevesse, T.; Gabriele, S., Spatial coordination between cell and nuclear shape within micropatterned endothelial cells, Nat. Commun., 671, 3, 1-11, (2012)
[50] Widlak, P.; Palyvoda, O.; Kumala, S.; Garrard, W. T., Modeling apoptotic chromatin condensation in normal cell nuclei requirement for intranuclear mobility and actin involvement, J. Biol. Chem., 277, 21683-21690, (2002)
[51] Williams, J. R.; Little, J. B.; Shipley, W. U., Association of Mammalian cell death with a specific endonucleolytic degradation of DNA, Nature, 252, 754-755, (1974)
[52] Willingham, M. C., Cytochemical methods for the detection of apoptosis, J. Histochem. Cytochem., 47, 1101-1109, (1999)
[53] Wyllie, A. H.; Kerr, J. F.; Currie, A. R., Cell death: the significance of apoptosis, Int. Rev. Cytol., 68, 251-306, (1980)
[54] Yang, W.; Gelles, J.; Musser, S. M., Imaging of single-molecule translocation through nuclear pore complexes, PNAS, 101, 12887-12892, (2004)
[55] Ye, H.; Cande, C.; Stephanou, N. C.; Jiang, S.; Gurbuxani, S.; Larochette, N.; Daugas, E.; Garrido, C.; Kroemer, G.; Wu, H., DNA binding is required for the apoptogenic action of apoptosis inducing factor, Nat. Struct. Mol. Biol., 9, 680-684, (2002)
[56] Yuste, V. J.; Sánchez-López, I.; Solé, C.; Moubarak, R. S.; Bayascas, J. R.; Dolcet, X.; Encinas, M.; Susin, S. A.; Comella, J. X., The contribution of apoptosis-inducing factor, caspase-activated dnase, and inhibitor of caspase-activated dnase to the nuclear phenotype and DNA degradation during apoptosis, J. Biol. Chem., 280, 35670-35683, (2005)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.