A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation

Journal of Cell Science

Volumn 119, Issue 11, 2006, Pages 2362-2374

  Moss, David K ^a   Betin, Virginie M ^a   Malesinski, Soazig D ^a,b   Lane, Jon D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Apoptosis; Chromatin; Fragmentation; Live cell imaging; Microtubules

Indexed keywords

ACTIN; CELL PROTEIN; GAMMA TUBULIN; MYOSIN; NINEIN; NOCODAZOLE; PACLITAXEL; PERICENTRIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL FRACTIONATION; CELL INTERACTION; CELL LINE; CENTROSOME; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IN VITRO STUDY; INTERPHASE; INTRACELLULAR TRANSPORT; MACROPHAGE; MICROTUBULE; MICROTUBULE ASSEMBLY; PHAGOCYTE; PRIORITY JOURNAL;

ANISOMYCIN; APOPTOSIS; CELL LINE; CHROMATIN; HELA CELLS; HUMANS; MACROPHAGES; MICROSCOPY, FLUORESCENCE; MICROTUBULES; ULTRAVIOLET RAYS;

EID: 33745505525     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02959     Document Type: Article

References (58)

1. Adrain, C., Duriez, P. J., Brumatti, G., Delivani, P. and Martin, S. J. (2006). The cytotoxic lymphocyte protease, granzyme B, targets the cytoskeleton and perturbs microtubule polymerization dynamics. J. Biol. Chem. 281, 8118-8125.
2. Baird, D. H., Myers, K. A., Mogensen, M., Moss, D. and Baas, P. W. (2004). Distribution of the microtubule-related protein ninein in developing neurons. Neuropharmacology 47, 677-683.
3. Bonanno, E., Ruzittu, M., Carla, E. C., Montinari, M. R., Pagliara, P. and Dini, L. (2000). Cell shape and organelle modification in apoptotic U937 cells. Eur. J. Histochem. 44, 237-246.
4. Bonfoco, E., Leist, M., Zhivotovsky, B., Orrenius, S., Lipton S. A. and Nicotern, P. (1996). Cytoskeletal breakdown and apoptosis elicited by NO donors in cerebellar granule cells require NMDA receptor activation. J. Neurochem. 67, 2484-2493.
5. Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34.
6. Byun, Y., Chen, F., Chang, R., Trivedi M, Green, K. J. and Cryns, V. L. (2001). Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ 8, 443-450.
7. Casciola-Rosen, L. A., Anhalt, G. and Rosen, A. (1994). Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179, 1317-1330.
8. Cosciola-Rosen, L., Rosen, A., Petri, M. and Schlissel, M. (1996). Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proc. Natl. Acad Sci. USA 93, 1624-1629.
9. Caulin, C., Salvesen, G. S. and Oshima, R. G. (1997). Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J. Cell Biol. 138,1379-1394.
10. Charras, G. T., Yarrow, J. C., Horton, M. A., Mahadevan, L. and Mitchison, T. J. (2005). Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435, 365-369.
11. Chen, F., Chang, R., Trivedi, M., Capetanaki, Y. and Cryns, V. L. (2003). Caspase proteolysis of desmin produces a dominant-negative inhibitor of intermediate filaments and promotes apoptosis. J. Biol. Chem. 278, 6848-6853.
12. Clarke, M. C., Savill, J., Jones, D. B., Noble, B. S. and Brown, S. B. (2003). Compartmentalized megakaryocyte death generates functional platelets committed to caspase-independent death. J. Cell Biol. 160, 577-587.
13. Cline, A. M. and Radic, M. Z. (2004). Marine lupus autoantibodies identify distinct subsets of apoptotic bodies. Autoimmunity 37, 85-93.
14. Coleman, M. L., Sahai, E. A., Yeo, M., Basch, M., Dewar, A. and Olson, M. F. (2001). Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345.
15. Cotter, T. G., Lennon, S. V., Glynn, J. M. and Green, D. R. (1992). Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res. 52, 997-1005.
16. Croft, D. R. Coleman, M. L., Li, S., Robertson, D., Sullivan, T., Stewart C. L. and Olson, M. F. (2005). Actin-myosin-based contraction is responsible for apoptotic nuclear disintegration. J Cell Biol. 168, 245-255.
17. De Botton, S., Sabri, S, Daugas, E., Zermati Y., Guidotti, J. E, Hermine, O., Kroemer, G., Vaincheaker, W. and Debili, N. (2002). Platelet formation is the consequence of caspase activation within megakaryocytes. Blood 100, 1310-1317.
18. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L. and Henson, P. M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
19. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A. and Henson, P. M. (2000). A receptor for phosphatidylserine-specific clearance of apoptatic cells. Nature 405, 85-90.
20. Fischer, U., Janicke, R. U. and Schulze-Osthoff, K. (2003). Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 10, 76-100.
21. Gerner, C., Frohwein, R, Gotzmann, J., Bayer, E., Gelbmann, D., Bursell, W. and Schulte-Hermann, R. (2000). The Fas-induced apoptosis analyzed by high throughput proteome analysis. J. Biol. Chem. 275, 39018-39026.
22. Hartwig, J. and Italiano, J., Jr (2003). The birth of the platelet. J. Thromb. Haemost. 1, 1580-1586.
23. Hoffmann, P. R., deCathelineau, A. M., Ogden, C. A., Leverrier, Y., Bratton, D. L., Daleke, D. L., Ridley, A. J., Fadok, V. A. and Henson, P. M. (2001). Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptatic cells. J Cell Biol. 155, 649-659.
24. Italiano, J. E., Jr, Lecine, P., Shivdasani, R. A. and Hartwig, J. H. (1999). Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J. Cell Biol. 147, 1299-1312.
25. Kerr, J. F,. Wyllie, A. H. and Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J. Cancer 26, 239-257.
26. Lane, J. and Allan, V. (1998). Microtubule-based membrane movement. Biochim. Biophys. Acta 1376, 27-55.
27. Lane, J. D., Vergnolle, M. A., Woodman, P. G. and Allan, V. J. (2001). Apoptotic cleavage of cytoplasmic dynein intermediate chain and p150(Glued) stops dynein-dependent membrane motility. J. Cell Biol. 153, 1415-1426.
28. Lane, J. D., Lucocq, J., Pryde, J., Barr, F. A, Woodman, P. G., Allan, V. J. and Lowe, M. (2002). Caspase-mediated cleavage of the stacking protein GRASP65 is required for Golgi fragmentation during apoptosis. J. Cell Biol. 156, 495-509.
29. Lane, J. D., Allan, V. J. and Woodman, P. G. (2005). Active relocation of chromatin and endoplasmic reticulum into blebs in late apoptotic cells. J. Cell Sci. 118, 4059-4071.
30. Lecine, F, Italiano, J. E., Jr, Kim, S. W., Villeval, J. L. and Shivdasani, R. A. (2000). Hematopoietic-specific beta 1 tubulin participates in a pathway of platelet biogenesis dependent on the transcription factor NF-E2. Blood 96, 1366-1373.
31. Leist, M. and Jaattela, M. (2001). Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2, 589-598.
32. Lowe, M, Lane, J. D., Woodman, P. G. and Allan, V. J. (2004). Caspase-mediated cleavage of syntaxin 5 and giantin accompanies inhibition of secretory traffic during apoptosis. J. Cell Sci. 117, 1139-1150.
33. Martin, S. J., Finucane, D. M., Amarante-Mendes, G. P., O'Brien, G. A. and Green, D. R. (1996). Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J. Biol. Chem 271, 28753-28756.
34. Maruta, H., Greer, K. and Rosenbaum, J. L. (1986). The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103, 571-579.
35. Mills, J. C., Lee, V. M. and Pittman, R. N. (1998a). Activation of a PP2A-like phosphatase and dephosphorylation of tau protein characterize onset of the execution phase of apoptosis. J. Cell Sci. 111, 625-636.
36. Mills, J. C., Stone, N. L. Erhardt, J. and Pittman, R. N. (1998b). Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J. Cell Biol. 140, 627- 636.
37. Mills, J. C., Stone, N. L. and Pittman, R. N. (1999). Extranuclear apoptosis. The role of the cytoplasm in the execution phase. J. Cell Biol. 146, 703-708.
38. Morrison, E. E, Wardleworth, B. N., Askham, J. M. Markham, A. F. and Meredith, D. M. (1998). EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 17, 3471-3477.
39. Morrison, E. E, Moncur, E M. and Askham, J. M. (2002). EB1 identifies sites of microtubule polymerisation during neurite development. Brain Res. Mol. Brain Res. 98, 145-152.
40. Ogden, C. A., deCathelineau, A, Hoffmann, P. R., Bratton, D., Ghebrehiwet, B., Fadok, V. A. and Henson, P M. (2001). C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194, 781-795.
41. Palazzo, A. F, Cook T. A., Alberts, A. S. and Gundersen, G. G. (2001). mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3, 723-729.
42. Pittman, S. M, Strickland, D. and Ireland, C. M. (1994). Polymerization of tubulin in apoptotic cells is not cell cycle dependent. Exp. Cell Res. 215, 263-272.
43. Pittman, S., Geyp, M, Fraser, M, Ellem, K, Peaston, A. and Ireland, C. (1997). Multiple centrosomal micrombule organising centres and increased microtubule stability are early features of VP-16-induced apoptosis in CCRF-CEM cells. Leuk Res. 21,491-499.
44. Rao, L., Perez, D. and White, E. (1996). Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135, 1441-1455.
45. Rodriguez, O. C., Schaefer, A. W., Mandato, C. A., Forscher, P., Bement, W. M. and Waterman-Storer, C. M. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599-609.
46. Rosen, A. and Casciola-Rosen, L. (2001). Clearing the way to mechanisms of autoimmunity. Nat. Med 7, 664-665.
47. Ruchaud, S, Korfali, N., Villa, P., Kottke, T. J., Dingwall, C. Kaufmann, S. H. and Earnshaw, W. C. (2002). Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 21, 1967-1977.
48. Savill, J. and Fadok, V. (2000). Corpse clearance defines the meaning of cell death. Nature 407, 784-788.
49. Savill, J., Dransfield, I., Gregory, C. and Haslett, C. (2002). A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975.
50. Sebbagh, M., Renvoize, C., Hamelin J, Riche, N., Bertoglio, J. and Breard, J. (2001). Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3, 346-352.
51. Sesso, A., Fujiwara, D. T., Jaeger, M., Jaeger, R., Li, T. C., Monteiro, M. M., Correa, H., Ferreira, M. A., Schumacher, R. I., Belisario, J. et a]. (1999). Structural elements common to mitosis and apoptosis. Tissue Cell 31, 357-371.
52. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299, 1743-1747.
53. Strasser, A., O'Connor, L. and Dixit, V. M. (2000). Apoptosis signaling. Annu. Rev. Biochem. 69, 217-245.
54. Su, L. K., Burrell, M, Hill, D. E., Gyuris, J, Brent, P, Wiltshire, R., Trent, J, Vogelstelln, B. and Kinzier, K. W. (1995). APC binds to the novel protein EB1. Cancer Res. 55, 2972-2977.
55. White, R. A, Pan, Z. and Salisbury, J. L. (2000). GFP-centrin as a marker for centriole dynamics in living cells. Microsc. Res. Teck 49, 451-457.
56. White, S. and Rosen, A. (2003). Apoptosis in systemic lupus erythematosus. Curr. Opin. Rheumatol. 15,557-562.
57. Wittmann, T, Bokoch, G. M. and Waterman-Storer, C. M. (2003). Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell Biol. 161, 845-851.
58. Young, A. Dictenberg, J. B, Purohit, A., Tuft, R. and Doxsey, S. J. (2000). Cytoplasmic dynein-mediated assembly of pericentrin and gamma tubulin onto centrosomes. Mol. Biol. Cell 11, 2047-2056.