Lamin proteolysis facilitates nuclear events during apoptosis

Journal of Cell Biology

Volumn 135, Issue 6, 1996, Pages 1441-1455

  Rao, Lakshmi ^a   Perez, Denise ^a   White, Eileen ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; INTERLEUKIN 1BETA CONVERTING ENZYME; LAMIN; LAMIN A; LAMIN C;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA DEGRADATION; HUMAN; HUMAN CELL; ONCOGENE; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADENOVIRUS E1B PROTEINS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BINDING SITES; CASPASE 1; CELL LINE; CELL NUCLEUS; CYSTEINE ENDOPEPTIDASES; DNA FRAGMENTATION; ENDOPEPTIDASES; ENZYME ACTIVATION; HELA CELLS; HUMANS; KINETICS; LAMIN TYPE A; LAMINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

ADENOVIRIDAE; RODENTIA;

EID: 0030465544     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1441     Document Type: Article

References (66)

1. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORTI/FADD-inleracling prolease, in Fas/APO-1-and TNF receptor-induced cell death. Cell. 85:803-815.
2. Boulakia, C.A., G. Chen, F.W.H. Ng, J.G. Teodoro, P.E. Branton, D.W. Nicholson, G.G. Poirier, and G.C. Shore. 1996. Bcl-2 and adenovirus E1B 19 kDA protein prevent ElA-induced processing of CPP32 and cleavage of poly(ADP-ribose)polymerase. Oncogene. 12:529-535.
3. Boyd, J.M., G.J. Gallo. B. Elangovan, A.B. Houghton, S. Malstrom, B.J. A very, R.G. Ebb, T. Subramanian, T. Chittenden, R.J. Lutz, and G. Chinnadurai. 1995. Bikl, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene. 11:1921-1928.
4. Chinnaiyan, A.M., K. Orth, K. O'Rourke, H. Duan, G.G. Poirier, and V.M. Dixit. 1996. Molecular ordering of the cell death pathway. J. Biol. Chem. 271:4573-4576.
5. Chiou, S.-K., L. Rao, and E. White. 1994a. Bcl-2 blocks p53-dependent apoptosis. Mol. Cell. Biol. 14:2556-2563.
6. Chiou, S.-K., C.C. Tseng, L. Rao, and E. White. 1994b. Functional complementation of the adenovirus E1B 19K protein with Bcl-2 in the inhibition of apoptosis in infected cells. J. Virol. 68:6553-6566.
7. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by El A which is inhibited by E1B. Genes & Dev. 7:546-554.
8. Duan, H., A.M. Chinnaiyan, P.L. Hudson. J.P. Wing, W. He, and V.M. Dixit. 1996. ICE-LAP3, a novel mammalian homologue of the Caenorhabditis elegans cell death protein Ced-3 is activated during Fas-and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 2713:1621-1625.
9. Earnshaw, W.C. 1995. Nuclear changes in apoptosis. Curr. Opin. Cell Biol. 1: 337-343.
10. Ellis, H., and H.R. Horvitz. 1986. Genetic control of programmed cell death in the nematode C. elegans. Cell. 44:817-829.
11. Ellis, H., J.-Y. Yuan, and H.R. Horvitz. 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7:663-698.
12. Faucheu, C., A. Diu, A.W.E. Chan, A.-M. Blanchet, C. Miossec, F. Herve, V. Collard-Dutilleul, Y. Gu, R.A. Aldape, J.A. Lippke, et al. 1995. A novel human protease similar to the interleukin-lβ converting enzyme induces apoptosis in transfected cells. EMBO (Eur. Mol Biol. Organ.) J. 14:1914-1922.
13. Fernandes-Alnemri, T., G. Litwack, and E. Alnemri. 1994. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-lβ-converting enzyme. J. Biol. Chem. 269:30761-30764.
14. Fernandes-Alnemri, T., G. Litwack, and E.S. Alnemri. 1995a. Mch2, a new member of the apoptotic Ced-3/lCE cysteine protease gene family. Cancer Res. 55:2737-2742.
15. Fernandes-Alnemri, T., A. Takahashi, R. Armstrong, J. Krebs, L. Fritz, K.J. Tomaselli, L. Wang, Z. Yu, C.M. Croce, G. Salveson, et al. 1995b. Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res. 55:6045-6052.
16. Fraser, A., and G. Evan. 1996. A license to kill. Celt. 85:781-784.
17. Glass, C.A., J.R. Glass, H. Taniura, K.W. Hasel, J. Blevitt, and L. Gerace. 1993. The α-helical rod domain of human lamins A and C contains a chromatin binding site. EMBO (Eur. Mol. Biol. Organ.) J, 12:4413-4424.
18. Han, J., P. Sabbatini, D. Ferez, L. Rao, D. Modha, and E. White. 1996a. The E1B 19K protein functions as an apoptosis inhibitor by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes & Dev, 10:461-477.
19. Han, J., P. Sabbatini, and E. White. 1996b. Induction of apoptosis by the E1B 19K binding protein, Nbk. Mol Cell Biol. 16:5857-5864.
20. Heald, R., and F. McKeon. 1990. Mutations of phosphorylation siles in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61:579-589.
21. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cultures. J. Mol. Biol. 26:365-369.
22. Kamens, J., M. Paskind, M. Huguinin. R.V. Talanian, H. Allen, D. Banach, N. Bump, M. Hackett, C.G. Johnston, P. Li, J.A. Mankovitch, M. Terranova, and T. Ghayur. 1995. Identification and characteriation of Ich-2, a novel member of the interleukin-lβ-converting enzyme family of cysteine proteases. J. Biol. Chem. 270:15250-15256.
23. Kaufmann, S.H. 1989. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothectin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49:5870-5878.
24. Kuida, K., J.A. Lippke, G. Ku, M.W. Harding, D.J. Livingston, M.S.-S. Su, and R.A. Flavell. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-lβ converting enzyme. Science (Wash. DC). 267:2000-2003.
25. Kumar, S., M. Kinoshita, M. Noda, N.G. Copeland, and N.A. Jenkins. 1994. Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-lβ-convertingenzyme. Genes & Dev. 8:1613-1626.
26. Lazebnik, Y.A., S.H. Kaufmann, S. Desnoyers, G.G. Poirier, and W.C. Earnshaw. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature (Lond.), 371:346-347.
27. Lazebnik, Y., A. Takahashi, R. Moir, R. Goldman, G. Poirier, S. Kaufmann, and W. Eamshaw. 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA. 92:9042-9046.
28. Li, P., A. Hamish, S. Banejee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-lβ-converting enzyme are defective in production of mature IL-lβ and resistant to endotoxic shock. Cell. 80:401-411.
29. Martin, J.S., and R.D. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell. 82:349-352.
30. Martinez, J., I. Georgoff, J. Martinez, and A.J. Levine. 1991. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes & Dev. 5:151-159.
31. McKeon, F. 1991. Nuclear lamin proteins: domains required for nuclear targeting, assembly, and cell-cycle-regulated dynamics. Curr. Opin. Cell Biol. 3:82-86.
32. McKeon, F.D., M.W. Kirschner, and D. Caput. 1988. Homolgies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature (Land.). 319:463-468.
33. Michalovitz, D., O. Halevy, and M. Oren. 1990. Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell. 62:671-681.
34. Miura, M., H. Zhu, R. Rotello, E.A. Hartwieg, and J. Yuan. 1993. Induction of apoptosis in fibroblasls by IL-lβ-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 75:653-660.
35. Moran, E. 1993. DNA tumor virus transforming proteins and the cell cycle. Curr. Opin. Genel. Dev. 3:63-70.
36. Munday, N.A., J.P. Vaillancourt, A. Ali. F.J. Casano, O.K. Miller, S.M. Molineaux, T.-T. Yamin, V.L. Yu, and D.W. Nicholson. 1995. Molecular cloning and pro-apoptotic activity of ICErel-II and ICErel-III, members of the ICE/ CED-3 family of cysteine proteases. J. Biol. Chem. 270:15870-15876.
37. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi. J.D. Bretz, M. Zhang, R. Gentz, et al. 1996. FLICE, A novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell. 85:817-827.
38. Neamati, N., A. Fernandez, S. Wright, J. Kiefer, and D.J. McConkey. 1995. Degradation of Lamin Bl precedes oligonucleosomal DNA fragmentation in apoptotic thymocytes and isolated thymocyte nuclei. J. Immunol. 154: 3788-3795.
39. Nicholson, D.W., A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle. Y.A. Lazebnik. et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Land.). 376:37-43.
40. Nigg, E.A. 1992. Assembly and cell cycle dynamics of the nuclear lamina. Semin. Cell Biol. 3:245-253.
41. Oberhammer, F.A., K. Hochegger, G Froschl, R. Tiefenbacher, and M. Pavelka. 1994. Chromatin condensation during apoptosis is accompanied by degradation of lamin A + B, without enhanced activation of cdc2 kinase. J. Cell Biol. 126:827-837.
42. Orth, K., M.A. Chinnaiyan, M. Garg, J.C. Froelich, and M.V. Dixit. 1996. The CED-3/1CE like protease Mch-2 is activated during apoptosis and cleaves the death substrate lamin A. J. Biol. Chem. 271:16720-16724.
43. Peter, M., J. Nakagawa, M. Doree, C.J. Labbe, and E.A. Nigg. 1990. In vitro disassembly of the nuclear lamina and M-phase specific phosphorylation of lamins by cdc-2. Cell. 61:591-602.
44. Pollard, M.J., K.L.E. Chan, J.B. Grant, F.K. Sullivan, M.E. Tan, and A.E. Glass. 1990. In vitro postlranslational modification of lamin B cloned from a human T-cell line. Mol. Cell Biol. 10:2164-2175.
45. Raff. M.C. 1992. Social controls on cell survival and cell death. Nature (Lond.). 356:398-400.
46. Rao, L., M. Debbas, P. Sabbatini, D. Hockenberry, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis which is inhibited by the E1B 19K and BcI-2 proteins. Prof. Natl. Acad. Sci. USA. 89:7742-7746.
47. Sabbatini, P., S.-K. Chiou, L. Rao, and E. White. 1995a. Modulation of p53mediated transcription and apoptosis by the adenovirus E1B 19K protein. Mol. Cell. Biol. 15:1060-1070.
48. Sabbatini, P., J. Lin, A.J. Levine, and E. White. 1995b. Essential role for p53mediated transcription in apoptosis but not growth suppression. Genes & Dev. 9:2184-2192.
49. Takahashi, A., E.S. Alnemri, Y.A. Lazebnik, T. Fernandes-Alnemri, G. Litwack, R.D. Moir, R.D. Goldman, G.G. Poirier, S.H. Kaufmann, and W.C. Earnshaw. 1996. Cleavage of lamin A by Mch2α but not CPP32: multiple ICE-related proteases with distinct substrate recognition properties are active in apoptosis. Proc. Natl. Acad. Sci. USA. 93:8395-8400.
50. Tewari, M., L.T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D.R. Beidler, G. Poirier, O.S. Salvesen, and V.M. Dixit. 1995, Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:801-809.
51. Thornberry, N.A., H.G. Bull, J.R. Calaycay, K.T. Chapman, A.D. Howard, M.J. Kostura, D.K. Miller, S.M. Molineaux, J.R. Weidner, and J. Aunins. 1992. A novel heterodimeric cysteine protease is required for interleukin-lβ processing in monocytes. Nature (Lond.). 356:768-774.
52. Ucker, D.S., J. Meyers, and P.S. Obermiller. 1992. Activation driven cell death: quantative differences alone distinguish stimuli triggering nontransformed T cell proliferation or death. J. Immunol. 149:1583-1592.
53. Wang, L., M. Miura, L. Bergeron, H. Zhu, and J. Yuan. 1994. lch-1, an ICE/ced3-related gene, encodes both positive and negative regulators of programmed cell death. Cell. 78:739-750.
54. Wang, Z.-Q., B. Auer, L. Stingl, H. Berghammer, D. Haidacher, M. Schweiger, and E.F. Wagner. 1995. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes & Dev. 9:509-520.
55. Ward, E.G., and W.M. Kirschner. 1990. Identification of cell cycle-regulated phosohorylation sites on nuclear lamin C. Cell. 61:561-577.
56. White, E. 1995. Regulation of p53-dependent apoptosis by E1A and E1B. In Current Topics in Microbiology and Immunology: The Molecular Repertoire of Adenovirus. W. Doerfler, editor. Springer Verlag, Berlin/Heidelberg. 199:33-58.
57. White, E. 1996. Life, death, and the pursuit of apoptosis. Genes & Dev. 10:1-15.
58. White, E., and R. Cipriani, 1989. Specific disruption of intermediate filaments and the nuclear lamina by the 19-kDa product of the adenovirus E1B oncogene, Proc. Natl. Acad. Sci. USA. 86:9886-9890.
59. White, E., T. Grodzieker, and B.W. Stillman. 1984. Mutations in the gene encoding the adenovirus E1B 19K tumor antigen cause degradation of chromosomal DNA.7. Virol. 52:410-419.
60. White, E., R. Cipriani, P. Sabbatini, and A. Denton. 1991. The adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of El A proteins. J. Virol. 65:2968-2978.
61. White, E., P. Sabbatini, M. Debbas, W.S.M. Wold, D.I. Kusher, and L. Gooding. 1992. The 19-kilodalton adenovirus El B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor a. Mol. Cell. Biol. 12:2570-2580.
62. White, E., L. Rao, S.-K. Chiou, C.-C. Tseng, P. Sabbalini, M. Gonzalez, and P. Venvaerde. 1994. Regulation of apoptosis by the transforming gene products of adenovirus. In Apoptosis. E. Mihich and R.T. Shimke, editors. Plenum Press, New York 47-62.
63. Whyte, M., and G. Evan. 1995. The last cut is the deepest. Nature (Lonil.). 376: 17-18.
64. Wyllie, A.M. 1980. Cell death: the significance of apoptosis. Int. Rev. Cvtol. 68: 251-306.
65. Yuan, J., S. Shaham, S. Ledoux, H.M. Ellis, and H.R. Horvitz. 1993. The C elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-lβ-converting enzyme. Cell. 75:641-652.
66. Zheng, H., D. Fletcher, W. Kozak, M. Jiang, K. Hofmann, C.A. Conn, D. Soszynski, C. Grablec, M. Trumbauer, A. Shaw, et al. 1995. Resistance to fever induction and impaired acute phase response in intcrleukin-lβ deficient mice. Immunity. 3:9-19.