NuMA and nuclear lamins behave differently in Fas-mediated apoptosis

Journal of Cell Science

Volumn 116, Issue 3, 2003, Pages 571-583

  Taimen, Pekka ^a   Kallajoki, Markku ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Apoptosis; Caspase independent; Caspases; Lamins; NuMA

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CASPASE; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE INHIBITOR; FAS ANTIGEN; LAMIN; LAMIN B; MATRIX PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; PROTEINASE; STAUROSPORINE;

APOPTOSIS; BREAST CANCER; CELL DEATH; CELL STRAIN MCF 7; CHROMATIN STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VIVO STUDY; LEUKEMIA CELL LINE; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; WESTERN BLOTTING;

MINK CELL FOCUS-FORMING VIRUS;

EID: 0037323898     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00227     Document Type: Review

References (51)

1. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T. and Saltiel, A. R. (1995). PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494.
2. Andrade, F., Roy, S., Nicholson, D., Thornberry, N., Rosen, A. and Casciola-Rosen, L. (1998). Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity 8, 451-460.
3. Bortul, R., Zweyer, M., Billi, A. M., Tabellini, G., Ochs, R. L., Bareggi, R., Cocco, L. and Martelli, A. M. (2001). Nuclear changes in necrotic HL-60 cells. J. Cell Biochem. 81, 19-31.
4. Casiano, C. A., Martin, S. J., Green, D. R. and Tan, E. M. (1996). Selective cleavage of nuclear autoantigens during CD95 (Fas/APO-I)-mediated T cell apoptosis. J. Exp. Med. 184, 765-770.
5. Compton, D. A. and Cleveland, D. W. (1993). NuMA is required for the proper completion of mitosis. J. Cell Biol. 120, 947-957.
6. Compton, D. A., Szilak, I. and Cleveland, D. W. (1992). Primary structure of NuMA, an intranuclear protein that defines a novel pathway for segregation of proteins at mitosis. J. Cell Biol. 116, 1395-1408.
7. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. and Nagata, S. (1998). A caspase-activated DNase that degrades DNA during apoptosis and its inhibitor ICAD. Nature 391, 43-50.
8. Foghsgaard, L., Wissing, D., Mauch, D., Lademann, U., Bastholm, L., Boes, M., Elling, F., Leist, M. and Jaattela, M. (2001). Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153, 999-1010.
9. Gaglio, T., Saredi, A. and Compton, D. A. (1995). NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 131, 693-708.
10. Gaglio, T., Saredi, A., Bingham, J. B., Hasbani, M. J., Gill, S. R., Schroer, T. A. and Compton, D. A. (1996). Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J. Cell Biol. 135, 399-414.
11. Germain, M., Affar, E. B., D'Amours, D., Dixit, V. M., Salvesen, G. S. and Poirier, G. G. (1999). Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 274, 28379-28384.
12. Gordon, M. B., Howard, L. and Compton, D. A. (2001). Chromosome movement in mitosis requires microtubule anchorage at spindle poles. J. Cell Biol. 152, 425-434.
13. Greidinger, E. L., Miller, D. K., Yamin, T. T., Casciola-Rosen, L. and Rosen, A. (1996). Sequential activation of three distinct ICE-like activities in Fas-ligated Jurkat cells. FEBS Lett. 390, 299-303.
14. Gueth-Hallonet, C., Weber, K. and Osborn, M. (1997). Cleavage of the nuclear matrix protein NuMA during apoptosis. Exp. Cell Res. 233, 21-24.
15. Gueth-Hallonet, C., Wang, J., Harborth, J., Weber, K. and Osborn, M. (1998). Induction of a regular nuclear lattice by overexpression of NuMA. Exp. Cell Res. 243, 434-452.
16. Guilly, M. N., Bensussan, A., Bourge, J. F., Bornens, M. and Courvalin, J. C. (1987). A human T lymphoblastic cell line lacks lamins A and C. EMBO J. 6, 3795-3799.
17. Harborth, J., Elbashir, S. M., Bechert, K., Tuschl, T. and Weber, K. (2001). Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 114, 4557-4565.
18. Harborth, J., Wang, J., Gueth-Hallonet, C., Weber, K. and Osborn, M. (1999). Self assembly of NuMA: multiarm oligomers as structural units of a nuclear lattice. EMBO J. 18, 1689-1700.
19. Hirata, H., Takahashi, A., Kobayashi, S., Yonehara, S., Sawai, H., Okazaki, T., Yamamoto, K. and Sasada, M. (1998). Caspases are activated in a branched protease cascade and control distinct downstream processes in Fas-induced apoptosis. J. Exp. Med. 187, 587-600.
20. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J. L., Schneider, P., Seed, B. and Tschopp, J. (2000). Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495.
21. Holmstrom, T. H., Tran, S. E., Johnson, V. L., Ahn, N. G., Chow, S. C. and Eriksson, J. E. (1999). Inhibition of mitogen-activated kinase signaling sensitizes HeLa cells to Fas receptor-mediated apoptosis. Mol. Cell Biol. 19, 5991-6002.
22. Hsu, H. L. and Yeh, N. H. (1996). Dynamic changes of NuMA during the cell cycle and possible appearance of a truncated form of NuMA during apoptosis. J. Cell Sci. 109, 277-288.
23. Jänicke, R. U., Ng, P., Sprengart, M. L. and Porter, A. G. (1998a). Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J. Biol. Chem. 273, 15540-15545.
24. Jänicke, R. U., Sprengart, M. L., Wati, M. R. and Porter, A. G. (1998b). Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273, 9357-9360.
25. Johnson, V. L., Ko, S. C., Holmstrom, T. H., Eriksson, J. E. and Chow, S. C. (2000). Effector caspases are dispensable for the early nuclear morphological changes during chemical-induced apoptosis. J. Cell Sci. 113, 2941-2953.
26. Kallajoki, M., Weber, K. and Osborn, M. (1991). A 210 kDa nuclear matrix protein is a functional part of the mitotic spindle; a microinjection study using SPN monoclonal antibodies. EMBO J. 10, 3351-3362.
27. Kallajoki, M., Weber, K. and Osborn, M. (1992). Ability to organize microtubules in taxol-treated mitotic PtK2 cells goes with the SPN antigen and not with the centrosome. J. Cell Sci. 102, 91-102.
28. Kallajoki, M., Harborth, J., Weber, K. and Osborn, M. (1993). Microinjection of a monoclonal antibody against SPN antigen, now identified by peptide sequences as the NuMA protein, induces micronuclei in PtK2 cells. J. Cell Sci. 104, 139-150.
29. Lazebnik, Y. A., Takahashi, A., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H. and Earnshaw, W. C. (1995). Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92, 9042-9046.
30. Luderus, M. E., den Blaauwen, J. L., de Smit, O. J., Compton, D. A. and van Driel, R. (1994). Binding of matrix attachment regions to lamin polymers involves single-stranded regions and the minor groove. Mol. Cell Biol. 14, 6297-6305.
31. Lyderson, B. K. and Pettyjohn, D. E. (1980). Human-spesific nuclear protein that associates with the polar region of the mitotic apparatus: Distribution in a human/hamster hybrid cell. Cell 22, 489-499.
32. Merdes, A. and Cleveland, D. W. (1998). The role of NuMA in the interphase nucleus. J. Cell Sci. 111, 71-79.
33. Merdes, A., Ramyar, K., Vechio, J. D. and Cleveland, D. W. (1996). A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447-458.
34. Nachury, M. V., Maresca, T. J., Salmon, W. C., Waterman-Storer, C. M., Heald, R. and Weis, K. (2001). Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95-106.
35. Nicholson, D. W. and Thornberry, N. A. (1997). Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
36. Orth, K., Chinnaiyan, A. M., Garg, M., Froelich, C. J. and Dixit, V. M. (1996). The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J. Biol. Chem. 271, 16443-16446.
37. Osborne, C. K., Hobbs, K. and Trent, J. M. (1987). Biological differences among MCF-7 human breast cancer cell lines from different laboratories. Breast Cancer Res. Treat. 9, 111-121.
38. Röber, R. A., Weber, K. and Osborn, M. (1989). Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365-378.
39. Sanghavi, D. M., Thelen, M., Thornberry, N. A., Casciola-Rosen, L. and Rosen, A. (1998). Caspase-mediated proteolysis during apoptosis: insights from apoptotic neutrophils. FEBS Lett. 422, 179-184.
40. Saredi, A., Howard, L. and Compton, D. A. (1996). NuMA assembles into an extensive filamentous structure when expressed in the cell cytoplasm. J. Cell Sci. 109, 619-630.
41. Slee, E. A., Adrain, C. and Martin, S. J. (2001). Executioner caspase-3, -6 and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol. Chem. 276, 7320-7326.
42. Sodja, C., Brown, D. L., Walker, P. R. and Chaly, N. (1998). Splenic T lymphocytes die preferentially during heat-induced apoptosis: NuMA reorganization as a marker. J. Cell Sci. 111, 2305-2313.
43. Stewart, C. and Burke, B. (1987). Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51, 383-392.
44. Taimen, P., Viljamaa, M. and Kallajoki, M. (2000). Preferential expression of NuMA in the nuclei of proliferating cells. Exp. Cell Res. 256, 140-149.
45. Takahashi, A., Alnemri, E. S., Lazebnik, Y. A., Fernandes-Alnemri, T., Litwack, G., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H. and Earnshaw, W. C. (1996). Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc. Natl. Acad Sci. USA 93, 8395-8400.
46. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S. and Dixit, V. M. (1995). Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809.
47. Weaver, V. M., Carson, C. E., Walker, P. R., Chaly, N., Lach, B., Raymond, Y., Brown, D. L. and Sikorska, M. (1996). Degradation of nuclear matrix and DNA cleavage in apoptotic thymocytes. J. Cell Sci. 109, 45-56.
48. Wiese, C., Wilde, A., Moore, M. S., Adam, S. A., Merdes, A. and Zheng, Y. (2001). Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291, 653-656.
49. Yang, C. H. and Snyder, M. (1992). The nuclear-mitotic apparatus protein is important in the establishment and maintenance of the bipolar mitotic spindle apparatus. Mol. Biol. Cell 3, 1259-1267.
50. Yang, C. H., Lambie, E. J. and Snyder, M. (1992). NuMA: an unusually long coiled-coil related protein in the mammalian nucleus. J. Cell Biol. 116, 1303-1317.
51. Zhang, D., Beresford, P. J., Greenberg, A. H. and Lieberman, J. (2001). Granzymes A and B directly cleave lamins and disrupt the nuclear lamina during granule-mediated cytolysis. Proc. Natl. Acad. Sci. USA 98, 5746-5751.