Alterations in cell nuclei during apoptosis

• Autorzy: Rogalinska M.
• Języki publikacji: EN

Abstrakty

EN

Apoptosis is a genetically programmed phenomenon that aids in maintaining homeostasis in multicellular organisms. The characteristic morphological features of apoptosis are highly conservative and are dependent on the cell type and the apoptotic inducer. The nuclear events occurring during apoptosis include changes at the molecular level (i.e. DNA cleavage, modifications of nuclear polypeptides, and proteolysis of several proteins important for cell maintenance), and, consequently, alterations at the morphological level (i.e. chromatin condensation, nuclear shrinkage, DNA fragmentation and apoptotic body formation). These events are still not fully understood. It is very probable that a progressive decrease in pH could also be an essential factor for the induction of nuclease and protease activities, and an important element of the optimal conditions for their function. This review details the current state of knowledge on apoptotic nuclear events, with particular focus on the proteins involved in the execution of apoptosis in cell nuclei, and on the differences in substrate cleavage profiles for different types of cell undergoing celi death.

Słowa kluczowe

EN

alteration; cell nucleus; apoptosis; DNA degradation; chromatin condensation; nuclear protein; proteolytic cleavage

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2002
• Tom: 07
• Numer: 4
• Opis fizyczny: p.995-1018,ref.

Twórcy

autor

Rogalinska M.

• Department of Cytobiochemistry, University of Lodz, Banacha 12/16, 90-237 Lodz, Poland

Bibliografia

• 1. Denecker, G., Vercammen, D., Declercq, W. and Vandenabeele, P. Apoptotic and necrotic cell death induced by death domain receptors. Cell. Mol. Life Sci. 58 (2001) 356-370.
• 2. Li, H., Zhu, H., Xu, C. and Yuan, J. Cleavage of Bid by caspase-8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501.
• 3. Jesenberg, V. and Jentsch, S. Deadly encounter: ubiquitin meets apoptosis. Nature Rev./Mol.Cell Biol. 3 (2002) 112-121.
• 4. Dini, L., Coppola, S., Ruzittu, M. T. and Ghibelli, L. Multiple pathways for apoptotic nuclear fragmentation. Exp. Cell Res. 223 (1996) 340-347.
• 5. Granville, D. J., Carthy, C. M., Hunt, D. W. C. and McManus B. M. Apoptosis: Molecular aspects of cell death and disease. Lab. Invest. 78 (1998) 893-913.
• 6. Wyllie, A. H., Kerr, J. F. R. and Currie, A. R. Cell death: The significance of apoptosis. Int. Rev. Cytol. 68 (1980) 251-306.
• 7. Falcieri, E., Zamai, L., Santi, S., Cinti, C., Gobbi, P., Bosco, D., Cataldi, A., Betts, C. and Vitale, M. The behaviour of nuclear domains in the course of apoptosis. Histochemistry 102 (1994) 221-231.
• 8. Nosseri, C., Coppola, S. and Ghibelli, L. Possible involvement of poly (ADP-ribosyl) polymerase in triggering stress-induced apoptosis. Exp. Cell Res. 212 (1994) 367-373.
• 9. Rao, L., Perez, D. and White, E. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135 (1996) 1441-1455.
• 10. Kaufmann, S. H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49 (1989) 5870-5878.
• 11. Krystosek, A. Preferential sites of early DNA cleavage in apoptosis and the pathway of nuclear damage. Histochem. Cell Biol. 111 (1999) 265-276.
• 12. Martin, S. J., Bradley, J. G. and Cotter, T. G. HL-60 cells induced to differentiate towards neutrophils subsequently die via apoptosis. Clin. Exp. Immunol. 79 (1990) 448-453.
• 13. Krajčí, D., Mareš, V., Lisá, V., Španová, A. and Vorlíček, J. Ultrastructure of nuclei of cisplatin-treated C6 glioma cells undergoing apoptosis. Eur. J. Cell Biol. 79 (2000) 365-376.
• 14. Mares, V., Giordano, P. A., Mazzini, G., Lisa, V., Pallicciari, C., Scherini, E., Bottiroli, G. and Drobnik, J. Influence of cis-dichlorodiammineplatinum on glioma cell morphology and cell cycle kinetics in tissue culture. Histochem. J. 19 (1987) 187-194.
• 15. Reed, C. J. Apoptosis and cancer: strategies for integrating programmed cell death. Semin. Hematol. 37 (2000) 9-16.
• 16. Horký, M., Wurzer, G., Kotala, V., Anton, M., Vojtešek, B., Vácha, J. and Wesierska-Gadek, J. Segregation of nucleolar components coincides with caspase-3 activation in cisplatin-treated HeLa cells. J. Cell Sci. 114 (2000) 663-670.
• 17. Maruyama, W., Irie, S. and Sato, T-A. Morphological changes in the nucleus and actin cytoskeleton in the process of Fas-induced apoptosis in Jurkat T cells. Histochem. J. 32 (2000) 495-503.
• 18. Liu, X., Zou, H., Slaughter, C. and Wang, X. DFF, a heterodimeric protein that functions downstreem of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89 (1997) 175-184.
• 19. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. and Nagata, S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391 (1998) 43-50.
• 20. Widłak, P. The DFF40/CAD endonuclease and its role in apoptosis. Acta Bioch. Polon. 47 (2000) 1037-1044.
• 21. Chang, H. Y. and Yang, X. Proteases for cell suicide: Functions and regulation of caspases. Microbiol. Mol. Biol. Rev. 64 (2000) 821-846.
• 22. Cryns, V. L. and Yuan, J. Y. Proteases to die for. Genes Dev. 12 (1998) 1551-1570.
• 23. Earnshaw, W. C. Nuclear changes in apoptosis. Curr. Op. Cell Biol. 7 (1995) 337-343.
• 24. Wang, K. K. W. Calpain and caspase: can you tell the difference? Trends Neurosci. 23 (2000) 20-26.
• 25. Ritter, P. M., Marti, A., Blanc, C., Baltzer, A., Krajewski, S., Reed, J. C. and Jaggi, R. Nuclear localization of procaspase-9 and processing by caspase-3- like activity in mammary epithelial cells. Eur. J. Cell Biol. 79 (2000) 358- 364.
• 26. Robertson, J. D., Orrenius, S. and Zhivitovsky, B. Nuclear events in apoptosis. J. Struct. Biol. 129 (2000) 346-358.
• 27. Johnson, V. L., Ko, S. C. W., Holmstrom, T. H., Eriksson, J. E. and Chow, S. C. Effector caspases are dispensable for the early nuclear morphological changes during chemical-induced apoptosis. J. Cell Sci. 113 (2000) 2941- 2953.
• 28. Zheng, T. S., Schlosser, S. F., Dao, T., Hingorani, R., Crispe, N., Boyer, J. L. and Flavel, R. A. Caspase-3 Controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc. Natl. Acad. Sci. USA 98 (1998) 13618-13623.
• 29. Graves, J., Yankee, T., Draves, K., Clark, E. and Krebs, E. Caspases: A signal transduction perspective. in: Protein modules in cellular signalling, (Heilmeyer, L. and Friedrich, P., Eds.) IOS Press, 2001, 374-383.
• 30. Burgoyne, L. A. The mechanisms of pycnosis: hypercondensation and death. Exp. Cell Res. 248 (1999) 214-222.
• 31. Kass, G. E. N., Eriksson, J. E., Weis, M., Orrenius, S. and Chow, S. C. Chromatin condensation during apoptosis requires ATP. Biochem. J. 318 (1996) 749-752.
• 32. Rogakou, E. P., Nieves-Neira, W., Boon, C., Pommier, Y. and Bonner, W. M. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2A.X histone at serine 139. J. Biol. Chem. 275 (2000) 9390-9395.
• 33. Kratzmeier, M., Albig, W., Hänecke, K. and Doenecke, D. Rapid dephosphorylation of H1 histones after apoptosis induction. J. Biol. Chem. 275 (2000) 30478-30486.
• 34. Th’ng, J. P. H. Histone modifications and apoptosis: cause or consequence? Biochem. Cell Biol. 79 (2001) 305-311.
• 35. Liu, X., Zou, H., Widlak, P., Garrard, W. T. and Wang, X. Activation of the apoptotic endonuclease DFF40 (caspase-activated DNase or nuclease). Oligomerization and direct interactions with histone H1. J. Biol. Chem. 274 (1999) 13836-13840.
• 36. Sahara, S., Aoto, M., Eguchi, Y., Imamoto, N., Yoneda, Y. and Tsujimoto, Y. Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature 401 (1999) 168-173.
• 37. Yasugi, E., Kumagai, T:, Nishikawa, Y., Okuma, E., Saeki, K., Oshima, M., Susin, S. A., Kroemer, G. and Yuo, A. Involvement of apoptosis-inducing factor during dolichyl monophosphate-induced apoptosis in U937 cells. FEBS Lett. 480 (2000) 197-200.
• 38. Liu, X., Li, P., Widlak, P., Zou, H., Luo, X., Garrard, W. T. and Wang, X. DFF40 induces DNA fragmentation and chromatin condensation during apoptosis. Proc. Natl. Acad. Sci. USA 95 (1998) 8461-8466.
• 39. Susin, S. A., Lorenzo, H. K., Zamzani, 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. and Kroemer, G. Molecular characterization of mitochondrial apoptosis-inducing factor. Naturę 397 (1999) 441-446.
• 40. Liu, X., Li, P., Widlak, P., Zou, H., Luo, X., Garrard, W. T. and Wang, X. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc. Natl. Acad. Sci. USA 95 (1998) 8461-8466.
• 41. Wyllie, A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 (1980) 555-556.
• 42. Huang, P. and Ballal, K. Biochemical characterization of the protein activity responsible for high molecular weight DNA fragmentation during drug-induced apoptosis. Cancer Res. 57 (1997) 3407-3414.
• 43. Ucker, D. S., Obermiller, P. S., Eckhart, W., Apgar, J. R., Berger, N. A. and Meyers, J. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol. Cell Biol. 12 (1992) 3060-3069.
• 44. Arruti, C., Chaudun, E., De Maria, A., Courtois, Y. and Counis, M. F. Characterisation of eye-lens DNases: long term persistence of activity in post apoptotic lens fibre cells. Cell Death Differ. 2 (1995) 47-56.
• 45. Widłak, P. and Garrard, W. T. Ionic and cofactor reąuirements for the activity of the apoptotic endonuclease DFF40/CAD. Mol. Cell Biochem. 218 (2001) 125-130.
• 46. Walker, P. R., LeBlanc, J. and Sikorska, M. Evidence that DNA fragmentation in apoptosis is initiated and propagated by single-strand breaks. Cell Death Differ. 4 (1997) 506-515.
• 47. Lips, J. and Kaina, B. DNA double-strand breaks trigger apoptosis in p53-deficient fibroblasts. Carcinogenesis 22 (2001) 579-585.
• 48. Lee, E., Furukubo, T., Mijabe, T., Yamauchi, A. and Kariya, K. Involvement of histone hyperacetylation in triggering DNA fragmentation of rat thymocytes undergoing apoptosis. FEBS Lett. 395 (1996) 183-187.
• 49. Sourlingas, T. G., Tsapali, D. S., Kaldis, A. D. and Sekeri-Pataryas, K. E. Histone deacetylase inhibitors induce apoptosis in peripheral blood lymphocytes along with histone H4 acetylation and the expression of the linker histone variant, H1°. Eur. J. Cell Biol. 80 (2001) 726-732.
• 50. Talasz, H., Helliger, W., Sarg, B., Debbage, P. L., Puschendorf, B. and Lindner, H. Hyperphosphorylation of histone H2A.X and dephosphorylation of histone H1 subtypes in the course of apoptosis. Cell Death Differ. 9 (2002) 27-39.
• 51. Li, T-K., Chen, A. Y., Yu, C., Mao, Y., Wang, H. and Liu, L. F. Activation of topoisomerase II-mediated excision of chromosomal DNA loops during oxidative stress. Genes Dev. 13 (1999) 1553-1560.
• 52. Lazebnik, Y. A., Takahashi, A., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H. and Earnshaw, W. C. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92 (1995) 9042-9046.
• 53. Hughes, F. M., Evans-Storms, R. B. and Cidlowski, J. A. Evidence that non-caspase proteases are required for chromatin degradation during apoptosis. Cell Death Differ. 5 (1998) 1017-1027.
• 54. Counis, M. F. and Torriglia, A. DNases and apoptosis. Biochem. Cell Biol. 78 (2000) 405-414.
• 55. Halenbeck, R., MacDonald, H., Roulston, A., Chen, T. T., Conroy, L. and Williams, L. T. CPAN, a human nuclase regulated by the caspase-sensitive inhibitor DFF45. Curr. Biol. 8 (1998) 537-540.
• 56. Sharif-Askari, E., Alam, A., Rhéaume, E., Beresford, P. J., Scotto, C., Sharma, K., Lee, D., deWolf, W. E., Nuttal, M. E., Lieberman, J. and Sékaly, R-P. Direct cleavage of the human DNA fragmentation factor-45 by granzyme B induces caspase-activated DNase release and DNA fragmantation. EMBO J. 20 (2001) 3101-3113.
• 57. Durrieu, F., Samejima, K., Fortune, J. M., Kandels-Lewis, S., Osheroff, N. and Earnshaw, W. C. DNA topoisomerase IIα interacts with CAD nuclease and is involved in chromatin condensation during apoptotic execution. Curr. Biol. 10 (2000) 923-926.
• 58. Cote, J. and Ruiz-Carrillo, A. Primers for mitochondrial DNA replication generated by endonuclease G. Science 261 (1993) 765-769.
• 59. van Loo, G., Schotte, P., van Gurp, M., Demol, H., Hoorelbeke, B., Gevaert, K., Rodriques, I., Ruiz-Carillo, A., Vandekerckhove, J., Declereq, W., Beyaert, R. and Vandenabeele, P. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ. 8 (2001) 1136-1142.
• 60. Gao, G. and Dou, Q. P. N-terminal cleavage of Bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes Bcl-2-independent cytochrome c release and apoptotic cell death. J. Cell Biochem. 80 (2000) 53-72.
• 61. Montague, J. W., Hughes, Jr F. M. and Cidlowski, J. A. Native recombinant cyclophilins A, B, and C degrade DNA independently of peptidylprolyl cis-trans isomerase activity: Potential roles of cyclophilins in apoptosis. J. Biol. Chem. 272 (1997) 6677-6684.
• 62. Moore, S. Pancreatic DNase. Enzymes 14 (1981) 281-296.
• 63. Torriglia, A., Chaudun, E., Chany-Fourier, F., Jeanny, J. C., Courtois, Y. and Counis, M. F. Involvement of DNase II in nuclear degeneration during lens cells differentiation. J. Biol. Chem. 270 (1995) 28579-28585.
• 64. Liu, Q. S., Pandey, S., Singh, R. K., Lin, W., Ribecco, M., Borowy-Borowski, H., Smith, B., LeBlanc, J., Walker, P. R. and Sikorska, M. DNase γ: a rat DNase I — like gene coding for a constitutively expressed chromatin-bound endonuclease. Biochemistry 37 (1998) 10134-10143.
• 65. Eastman, A. Deoxyribonuclease II in apoptosis and the significance of intracellular acidification. Cell Death Differ. 1 (1994) 7-9.
• 66. Furlong, I. J., Ascaso, R., Lopez Rivas, A. and Collins, M. K. L. Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J. Cell Sci. 110 (1997) 653-661.
• 67. Fraser, M. J., Tynan, S. J., Papaioannou, A., Ireland, C. M. and Pittman, S. M. Endo-exonuclease of human leukaemic cells: evidence for a role in apoptosis. J. Celi Sci. 109 (1996) 2343-2360.
• 68. Meng, X. W., Fraser, M. J., Feller, J. M. and Ziegler, J. B. Caspase-3 activates endo-exonuclease: Further evidence for a role of the nuclease in apoptosis. Apoptosis 5 (2000) 243-254.
• 69. Torriglia, A., Perani, P., Brossas, J. Y., Chaudun, E., Treton, J., Courtois, Y. and Counis, M. F. L-DNase II, a molecule that links proteases and endonucleases in apoptosis, derives from the ubiquitous serpin Leukocute Elastase Inhibitor. Mol. Cell Biol. 18 (1998) 3612-3619.
• 70. Holdenrieder, S., Stieber, P., Bodenmüller, H., Busch, M., Fertig, G., Fürst, H., Schalhorn, A., Schmeller, N., Untch, M. and Seidel, D. Nucleosomes in serum of patients with benign and malignant diseases. Int. J. Cancer (Pred. Oncol.) 95 (2001) 114-120.
• 71. Berger, N. A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 101 (1985) 4-15.
• 72. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E. and Poirier, G. G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53 (1993) 3976-3985.
• 73. Scovassi, I. A. and Poirier, G. G. Poly (ADP-ribosylation) and apoptosis. Molec. Cell Bioch. 199 (1999) 125-137.
• 74. Herceg, Z. and Wang, Z-Q. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomie integrity and cell death. Mutation Res. 477 (2001) 97-110.
• 75. Shimizu, T., Kubota, M., Tanizawa, A., Sano, H., Kasai, Y., Hashimoto, H., Akiyama, Y. and Mikawa, H. Inhibition of both etoposide-induced fragmentation and activation of poly(ADP-ribose) synthesis by zinc ion. Biochem. Biophys. Res. Commun. 169 (1990) 1172-1177.
• 76. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G and Earnshaw, W. C. Cleavage of poly(ADP-ribose) polymerase by protease with properties like ICE. Nature 371 (1994) 346-347.
• 77. Decker, P., Isenberg, D. and Muller, S. Inhibition of caspase-3-mediated poly-(ADP-ribose) polymerase PARP apoptotic cleavage by human PARP autoantibodies and effect on cells undergoing apoptosis. J. Biol. Chem. 275 (2000) 9043-9046.
• 78. Margolin, N., Raybuch, S. A., Wilson, K. P., Chen, W., Fox, T., Gu, Y. and Livingston DJ. Substrate and inhibitor specificity of interleukin-1β- converting enzyme and related caspases. J. Biol. Chem. 272 (1997) 7223- 7228.
• 79. Fernandes-Alnemri, T., Litwack, G. and Alnemri, E. S. Mch2, a new member of the apoptotic ced-3 ICE cysteinę protease gene family. Cancer Res. 55 (1995) 2737-2742.
• 80. Gu, Y., Sarnecki, C., Aldape, R. A, Livingston, D. J. and Su, M. J. Cleavage of poly(ADP-ribose) polymerase by interleukin-1 β converting enzyme and its homologs TX and Nedd-2. J. Biol. Chem. 270 (1995) 18715-18718.
• 81. D'Amous, D., Germain, M., Orth, K., Dixit, V. M. and Poirier, G. G. Proteolysis of poly(ADP-ribose) polymerase by caspase-3: kinetics of cleavage of mono(ADP-ribosyl)ated and DNA-bound substrates. Radiation Res. 150 (1998) 3-10.
• 82. Wang, Z-Q., Stingl, L., Morrison, C., Jantsch, M., Los, M., Schultze-Osthoff, K. and Wagner, E. F. PARP is important for genomic stability but dispensible in apoptosis. Genes Dev. 11 (1997) 2347-2358.
• 83. Scovassi, A. I., Denegri, M., Donzelli, M., Rossi, L., Bernardi, R., Mandarino, A., Frouin, I. and Negri, C. Poly(ADP-ribose) synthesis in cells undergoing apoptosis: an attempt to face death before PARP degradation. Eur. J. Histochem. 4 (1998) 251-258.
• 84. Moir, R. D., Spann, T. P. and Goldmann R. D. The dynamic properties and possible functions of nuclear lamins. Int. Rev. Cytol. 162B (1995) 141-182.
• 85. Benevente, R. and Krone, G. Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies. J. Cell Biol. 103 (1986) 1847-1854.
• 86. Stuurman, N., Heins, S. and Aebi, U. Nuclear lamins: their structure, assembly, and interactions. J. Struct. Biol. 122 (1998) 42-66.
• 87. Goldman, A., Moir, R., Stewart, M. and Goldman, R. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J. Cell Biol. 4 (1992) 725-735.
• 88. Gant, T. M. and Wilson, K. L. Nuclear assembly. Annu. Rev. Cell Dev. Biol. 13 (1997) 669-695.
• 89. Zewe, M., Hoger, T. H., Fink, T., Lichter, P., Krohne, G. and Franke, W. W. Gene structure and chromosomal localization of the murine lamin B2 gene. Eur. J. Cell Biol. 56 (1991) 342-350.
• 90. Zhivotovsky, B., Gahm, A. and Orrenius, S. Two different proteases are involved in the proteolysis of lamin during apoptosis. Bioch. Biophys. Res. Commun. 233 (1997) 96-101.
• 91. Dynlacht, J. R., Roberts, Z. V., Earles, M., Henthorn, J. and Seno, J. D. Different patterns of DNA fragmentation and degradation of nuclear matrix proteins during apoptosis induced by radiation, hyperthermia or etoposide. Radiation Res. 154 (2000) 515-530.
• 92. Oberhammer, F. A., Hochegger, K., Fröschl, G. and Tiefenbach, R. Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase. J. Cell Biol. 126 (1994) 827-837.
• 93. Duband-Goulet, I., Courvalin, J-C. and Buendia, B. LBR, a chromatin and lamin binding protein from the inner nuclear membrane, is proteolysed at late stages of apoptosis. J. Cell Sci. 111 (1998) 1441-1451.
• 94. Cross, T., Griffiths, G., Deacon, E., Sallis, R., Gough, M., Watters, D. and Lord, J. M. PCK-δ is an apoptotic lamin kinase. Oncogen 19 (2000) 2331-2337.
• 95. Emoto, Y., Manome, Y., Meinhardt, G., Kisaki, H., Kharbanda, S., Robertson, M., Ghayur, T., Wong, W. W., Kamen, R., Weichselbaum, R. and Kufe, D. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 14 (1995) 6148-6156.
• 96. Ghayur, T., Hugunin, M., Talanian, R. V., Ratnovsky, S., Quinlan, C., Emoto, Y., Pandey, P., Datta, R., Kharbanda, S., Allen, H., Kamen, R., Wong, W. and Kufe, D. Proteolytic activation of protein kinase C delta by an ICE/CED-3 like protease induces characteristics of apoptosis. J. Exp. Med. 184 (1996) 2399-2404.
• 97. Chu, A., Rossadi, R. and Stochaj, U. Velcro in the nuclear envelope: LBR and LAPs. FEBS Lett. 441 (1998) 165-169.
• 98. Lydersen, B. K. and Pettijohn, D. E. Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell 22 (1980) 489-499.
• 99. Harborth, J., Weber, K. and Osborn, M. Epitope mapping and direct visualization of the parralel, in-register arrangement of the double-stranded coiled-coil in the NuMA protein. EMBO J. 14 (1995) 2447-2460.
• 100. Gaglio, T., Saredi, A. and Compton, D. A. NuMA is reąuired for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 131 (1995) 693-708. Li, H. and Yuan, J. Deciphering the pathways of life and death. Curr. Op. Cell Biol. 11 (1999) 261-266.
• 101. Merdes, A. and Cleveland, D. W. The role of NuMA in interphase nucleus. J. Cell Sci. 111 (1998) 71-79.
• 102. Martelli, A. M., Zweyer, M., Ochs, R. L., Tazzari, P. L., Talbellini, G., Narducci, P. and Bortul, R. Nuclear apoptotic changes: an overview. J. Cell Bioch. 82 (2001) 634-646.
• 103. Keesee, S. K., Briggman, J. V., Thill, G. and Wu, Y-J. Utilization of nuclear matrix proteins for cancer. Crit. Rev. Euk. Gene Exp. 6 (1996) 189-214.
• 104. Miller, T. E., Beausang, L. A., Meneghini, M. and Lidgard, G. Death-induced changes to the nuclear matrix: the use of anti-nuclear matrix antibodies to study on agents of apoptosis. Biotechniques 15 (1993) 1042-1047.
• 105. Miller, T. E., Beausang, L. A., Winchel, L. F. and Lidgard, GP. Detection of nuclear matrix proteins in serum from cancer patients. Cancer Res. 52 (1992) 422-427.
• 106. Bortul, R., Zweyer, M., Billi, A. M., Tabellini, G., Ochs, R. L., Bareggi, R., Cocco, L. and Martelli, A. M. Nuclear changes in necrotic HL-60 cells. J. Cell Biochem. (Suppl.) 36 (2001) 19-31.
• 107. Shah, G. M., Shah, R. G. and Poirier, G. G. Different cleavage pattern for poly(ADP-ribose) polymerase during necrosis and apoptosis in HL-60 cells. Biochem. Biophys. Res. Commun. 229 (1996) 838-844.
• 108. Casiano, C. A., Ochs, R. L. and Tan, E. M. Distinct cleavage products of nuclear protein in apoptosis and necrosis revealed by autoantibody probes. Cell Death Differ. 5 (1998) 183-190.
• 109. Berret, T. J. and Spelsberg, T. C. Nuclear matrix and steroid hormone action. Vitam. Horm. 55 (1999) 127-163.
• 110. Blomgren, K., Zhu, C., Wang, X., Karlsson, J-O., Leverin A-L., Bahr, B. A., Mallard, C. and Hagberg, H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia. J. Biol. Chem. 276 (2001) 10191-10198.
• 111. Nunez, G., Benedict, M. A., Hu, Y. and Inohara, N. Caspases: the proteases of the apoptotic pathway. Oncogene 17 (1998) 3237-3245.
• 112. Faleiro, L. and Lazebnik, Y. Caspases disrupt the nuclear-cytoplasmic barrier. J. Cell Biol. 151 (2000) 951-959.
• 113. Buendia, B., Santa-Maria, A. and Courvalin, J. C. Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis. J. Cell Sci. 112 (1999) 1743-1753.
• 114. Ohtsubo, T., Park, H. J., Lyons, J. C., Ohnishi, T. and Song, C. W. Effect of acidic environment and p53 on apoptosis induction by hyperthermia. Int. J. Hyperthermia 16 (2000) 481-491.