Mammalian CLASP1 and CLASP2 cooperate to ensure mitotic fidelity by regulating spindle and kinetochore function

Molecular Biology of the Cell

Volumn 17, Issue 10, 2006, Pages 4526-4542

  Pereira, Ana L ^a,b   Pereira, António J ^a   Maia, Ana R R ^a   Drabek, Ksenija ^b   Sayas, C Laura ^b   Hergert, Polla J ^c   Lince Faria, Mariana ^a   Matos, Irina ^a   Duque, Cristina ^e   Stepanova, Tatiana ^b   Rieder, Conly L ^c   Earnshaw, William C ^d   Galjart, Niels ^b   Maiato, Helder ^a,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c WADSWORTH CENTER   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e University of Porto   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE PROTEIN; PROTEIN CLASP1; PROTEIN CLASP2; UNCLASSIFIED DRUG;

ANAPHASE; ANEUPLOIDY; ANIMAL CELL; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CELL VIABILITY; CENTROMERE; CENTROSOME; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; DROSOPHILA; DYNAMICS; FIBROBLAST; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MAMMAL; MICROTUBULE; MITOSIS SPINDLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; REGULATORY MECHANISM; XENOPUS; YEAST;

ANEUPLOIDY; ANIMALS; CELLS, CULTURED; CENTROSOME; HELA CELLS; HUMANS; KINETOCHORES; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; TRANSFECTION;

MAMMALIA;

EID: 33749480148     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-07-0579     Document Type: Article

References (58)

1. Akhmanova, A., and Hoogenraad, C. C. (2005). Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17, 47-54.
2. Akhmanova, A., et al. (2001). Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
3. Akhmanova, A., et al. (2005). The microtubule plus-end-tracking protein CLIP-170 associates with the spermatid manchette and is essential for spermatogenesis. Genes Dev. 19, 2501-2515.
4. Amin-Hanjani, S., and Wadsworth, P. (1991). Inhibition of spindle elongation by taxol. Cell Motil. Cytoskeleton 20, 136-144.
5. Ault, J. G., DeMarco, A. J., Salmon, E. D., and Rieder, C. L. (1991). Studies on the ejection properties of asters: astral microtubule turnover influences the oscillatory behavior and positioning of mono-oriented chromosomes. J. Cell Sci. 99, 701-710.
6. Bilbe, G., et al. (1992). Restin: a novel intermediate filament-associated protein highly expressed in the Reed-Sternberg cells of Hodgkin's disease. EMBO J. 11, 2103-2113.
7. Brito, D. A., and Rieder, C. L. (2006). Mitotic checkpoint slippage in humans occurs via Cyclin B destruction in the presence of an active checkpoint. Curr. Biol. 16, 1194-1200.
8. Brust-Mascher, I., Civelekoglu-Scholey, G., Kwon, M., Mogilner, A., and Scholey, J. M. (2004). Model for anaphase B: role of three mitotic motors in a switch from poleward flux to spindle elongation. Proc. Natl. Acad. Sci. USA 101, 15938-15943.
9. Bu, W., and Su, L. K. (2001). Regulation of microtubule assembly by human EB1 family proteins. Oncogene 20, 3185-3192.
10. Cande, W. Z. (1982). Nucleotide requirements for anaphase chromosome movements in permeabilized mitotic cells: anaphase B but not anaphase A requires ATP. Cell 28, 15-22.
11. Cande, W. Z., McDonald, K., and Meeusen, R. L. (1981). A permeabilized cell model for studying cell division: a comparison of anaphase chromosome movement and cleavage furrow constriction in lysed PtK1 cells. J. Cell Biol. 88, 618-629.
12. Cheeseman, I. M., MacLeod, I., Yates, J. R., 3rd, Oegema, K., and Desai, A. (2005). The CENP-F-like proteins HCP-1 and HCP-2 target CLASP to kinetochores to mediate chromosome segregation. Curr. Biol. 15, 771-777.
13. Cimini, D., and Degrassi, F. (2005). Aneuploidy: a matter of bad connections. Trends Cell Biol. 15, 442-451.
14. Cooke, C. A., Schaar, B., Yen, T. J., and Earnshaw, W. C. (1997). Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma 106, 446-455.
15. De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., Aerts, F., and De Mey, J. (1986). Microtubule dynamics during the cell cycle: the effects of taxol and nocodazole on the microtubule system of Pt K2 cells at different stages of the mitotic cycle. Int. Rev. Cytol. 101, 215-274.
16. Desai, A., Rybina, S., Muller-Reichert, T., Shevchenko, A., Hyman, A., and Oegema, K. (2003). KNL-1 directs assembly of the microtubule-binding interface of the kinetochore in C. elegans. Genes Dev. 17, 2421-2435.
17. Draviam, V. M., Shapiro, I., Aldridge, B., and Sorger, P. K. (2006). Misorientation and reduced stretching of aligned sister kinetochores promote chromosome missegregation in EB1- or APC-depleted cells. EMBO J. 25, 2814-2827.
18. Emanuele, M. J., McCleland, M. L., Satinover, D. L., and Stukenberg, P. T. (2005). Measuring the stoichiometry and physical interactions between components elucidates the architecture of the vertebrate kinetochore. Mol. Biol. Cell 16, 4882-4892.
19. Fodde, R., et al. (2001). Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3, 433-438.
20. Fu, J. F., Hsu, H. C., and Shih, L. Y. (2005). MLL is fused to EB1 (MAPRE1), which encodes a microtubule-associated protein, in a patient with acute lymphoblastic leukemia. Genes Chromosomes Cancer 43, 206-210.
21. Fujiwara, T., Bandi, M., Nitta, M., Ivanova, E. V., Bronson, R. T., and Pellman, D. (2005). Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043-1047.
22. Ganem, N. J., Upton, K., and Compton, D. A. (2005). Efficient mitosis in human cells lacking poleward microtubule flux. Curr. Biol. 15, 1827-1832.
23. Gönczy, P., et al. (2000). Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408, 331-336.
24. Gorbsky, G. J., Sammak, P. J., and Borisy, G. G. (1987). Chromosomes move poleward in anaphase along stationary microtubules that coordinately disassemble from their kinetochore ends. J. Cell Biol. 104, 9-18.
25. Green, R. A., and Kaplan, K. B. (2003). Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J. Cell Biol. 163, 949-961.
26. Green, R. A., Wollman, R., and Kaplan, K. B. (2005). APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol. Biol. Cell 16, 4609-4622.
27. Hannak, E., and Heald, R. (2006). Xorbit/CLASP links dynamic microtubules to chromosomes in the Xenopus meiotic spindle. J. Cell Biol. 172, 19-25.
28. Hoffman, D. B., Pearson, C. G., Yen, T. J., Howell, B. J., and Salmon, E. D. (2001). Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12, 1995-2009.
29. Inoue, Y. H., do Carmo Avidesqq, M., Shiraki, M., Deak, P., Yamaguchi, M., Nishimoto, Y., Matsukage, A., and Glover, D. M. (2000). Orbit, a novel microtubule-associated protein essential for mitosis in Drosophila melanogaster. J. Cell Biol. 149, 153-166.
30. Inoue, Y. H., Savoian, M. S., Suzuki, T., Mathe, E., Yamamoto, M. T., and Glover, D. M. (2004). Mutations in orbit/mast reveal that the central spindle is comprised of two microtubule populations, those that initiate cleavage and those that propagate furrow ingression. J. Cell Biol. 166, 49-60.
31. Jordan, M. A., Toso, R. J., Thrower, D., and Wilson, L. (1993). Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. USA 90, 9552-9556.
32. Kaplan, K. B., Burds, A. A., Swedlow, J. R., Bekir, S. S., Sorger, P. K., and Nathke, I. S. (2001). A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat. Cell Biol. 3, 429-432.
33. Khodjakov, A., and Rieder, C. L. (2001). Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153, 237-242.
34. Komarova, Y., Lansbergen, G., Galjart, N., Grosveld, F., Borisy, G. G., and Akhmanova, A. (2005). EB1 and EB3 control CLIP dissociation from the ends of growing microtubules. Mol. Biol. Cell, 16, 5334-5345.
35. Lemos, C. L., Sampaio, P., Maiato, H., Costa, M., Omel'yanchuk, L. V., Liberal, V., and Sunkel, C. E. (2000). Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO J. 19, 3668-3682.
36. Maiato, H., DeLuca, J., Salmon, E. D., and Earnshaw, W. C. (2004). The dynamic kinetochore-microtubule interface. J. Cell Sci. 117, 5461-5477.
37. Maiato, H., Fairley, E. A., Rieder, C. L., Swedlow, J. R., Sunkel, C. E., and Earnshaw, W. C. (2003a). Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 113, 891-904.
38. Maiato, H., Khodjakov, A., and Rieder, C. L. (2005). Drosophila CLASP is required for the incorporation of microtubule subunits into fluxing kinetochore fibres. Nat. Cell Biol. 7, 42-47.
39. Maiato, H., Rieder, C. L., Earnshaw, W. C., and Sunkel, C. E. (2003b). How do kinetochores CLASP dynamic microtubules? Cell Cycle 2, 511-514.
40. Maiato, H., Sampaio, P., Lemos, C. L., Findlay, J., Carmena, M., Earnshaw, W. C., and Sunkel, C. E. (2002). MAST/Orbit has a role in microtubule-kinetochore attachment and is essential for chromosome alignment and maintenance of spindle bipolarity. J. Cell Biol. 157, 749-760.
41. Mimori-Kiyosue, Y., et al. (2005). CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168, 141-153.
42. Nakagawa, H., Koyama, K., Murata, Y., Morito, M., Akiyama, T., and Nakamura, Y. (2000). EB3, a novel member of the EB1 family preferentially expressed in the central nervous system, binds to a CNS-specific APC homologue. Oncogene 19, 210-216.
43. Nathke, I. S. (2004). The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu. Rev. Cell Dev. Biol. 20, 337-366.
44. Pasqualone, D., and Huffaker, T. C. (1994). STU1, a suppressor of a beta-tubulin mutation, encodes a novel and essential component of the yeast mitotic spindle. J. Cell Biol. 127, 1973-1984.
45. Rajagopalan, H., and Lengauer, C. (2004). Aneuploidy and cancer. Nature 432, 338-341.
46. Rieder, C. L., and Cassels, G. (1999). Correlative light and electron microscopy of mitotic cells in monolayer cultures. Methods Cell Biol. 61, 297-315.
47. Rieder, C. L., and Maiato, H. (2004). Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev. Cell 7, 637-651.
48. Rogers, G. C., Rogers, S. L., and Sharp, D. J. (2005). Spindle microtubules in flux. J. Cell Sci. 118, 1105-1116.
49. Shelden, E., and Wadsworth, P. (1990). Interzonal microtubules are dynamic during spindle elongation. J. Cell Sci. 97, 273-281.
50. Skop, A. R., Liu, H., Yates, J., 3rd, Meyer, B. J., and Heald, R. (2004). Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 305, 61-66.
51. Sluder, G., Thompson, E. A., Miller, F. J., Hayes, J., and Rieder, C. L. (1997). The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J. Cell Sci. 110, 421-429.
52. Tanenbaum, M. E., Galjart, N., van Vugt, M. A., and Medema, R. H. (2006). CLIP-170 facilitates the formation of kinetochore-microtubule attachments. EMBO J. 25, 45-57.
53. Tighe, A., Johnson, V. L., and Taylor, S. S. (2004). Truncating APC mutations have dominant effects on proliferation, spindle checkpoint control, survival and chromosome stability. J. Cell Sci. 117, 6339-6353.
54. Tonini, T., Claudio, P. P., Giordano, A., and Romano, G. (2004). Transient production of retroviral- and lentiviral-based vectors for the transduction of Mammalian cells. Methods Mol. Biol. 285, 141-148.
55. van der Wegen, P., Louwen, R., Imam, A. M., Buijs-Offerman, R. M., Sinaasappel, M., Grosveld, F., and Scholte, B. J. (2006). Successful treatment of UGT1A1 deficiency in a rat model of Crigler-Najjar disease by intravenous administration of a liver-specific lentiviral vector. Mol. Ther. 13, 374-381.
56. van Es, J. H., Kirkpatrick, C., van de Wetering, M., Molenaar, M., Miles, A., Kuipers, J., Destree, O., Peifer, M., and Clevers, H. (1999). Identification of APC2, a homologue of the adenomatous polyposis coli tumour suppressor. Curr. Biol. 9, 105-108.
57. Wadsworth, P., Shelden, E., Rupp, G., and Rieder, C. L. (1989). Biotin-tubulin incorporates into kinetochore fiber microtubules during early but not late anaphase. J. Cell Biol. 109, 2257-2265.
58. Weaver, B. A., and Cleveland, D. W. (2005). Decoding the links between mitosis, cancer, and chemotherapy: the mitotic checkpoint, adaptation, and cell death. Cancer Cell 8, 7-12.