Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms

Journal of Cell Science

Volumn 116, Issue 20, 2003, Pages 4213-4225

  Cimini, Daniela ^a   Moree, Ben ^a   Canman, Julie C ^a   Salmon, E D ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Chromosome segregation; Lagging chromosomes; Merotelic orientation; Mitotic checkpoint

Indexed keywords

NOCODAZOLE;

ANAPHASE; ANIMAL CELL; ANIMAL TISSUE; CENTROMERE; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; CYTOLOGY; MAMMAL CELL; METAPHASE CHROMOSOME; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS INHIBITION; MITOSIS SPINDLE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REVIEW; SPINDLE POLE BODY;

ANAPHASE; ANIMALS; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOME SEGREGATION; HUMANS; KINETOCHORES; METAPHASE; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; NOCODAZOLE; REPRESSOR PROTEINS;

ANIMALIA; MAMMALIA;

EID: 0242287897     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00716     Document Type: Review

References (55)

1. Adams, R. R., Maiato, H., Earnshaw, W. C. and Carmena, M. (2001). Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153, 865-880.
2. Ault, J. G. and Rieder, C. L. (1992). Chromosome mal-orientation and reorientation during mitosis. Cell Motil. Cytoskeleton 22, 155-159.
3. Bajer, A. S. and Molè-Bajer, J. (1972). Hypotheses of chromosome movements and spindle structures. Int. Rev. Cyt. Suppl. 3, 177-215.
4. Biggins, S. and Murray, A. W. (2001). The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev. 15, 3118-3129.
5. Canman, J., Salmon, E. and Fang, G. (2002a). Inducing Precocious Anaphase in Cultured Mammalian Cells. Cell Motil. Cytol. 52, 61-65.
6. Canman, J. C., Sharma, N., Straight, A., Shannon, K. B., Fang, G. and Salmon, E. D. (2002b). Anaphase onset does not require the microtubule-dependent depletion of kinetochore and centromere-binding proteins. J. Cell Sci. 115, 3787-3795.
7. Cassimeris, L., Rieder, C. L., Rupp, G. and Salmon, E. D. (1990). Stability of microtubule attachment to metaphase kinetochores in PtK1 cells. J. Cell Sci. 96, 9-15.
8. Catalan, J., Falck, G. C. and Norppa, H. (2000). The X chromosome frequently lags behind in female lymphocyte anaphase. Am. J. Hum. Genet. 66, 687-691.
9. Church, K. and Lin, H. P. (1982). Meiosis in Drosophila melanogaster. II. The prometaphase-I kinetochore microtubule bundle and kinetochore orientation in males. J. Cell Biol. 93, 365-373.
10. Cimini, D., Fioravanti, D., Salmon, F. D. and Degrassi, F. (2002). Merotelic kinetochore orientation versus chromosome mono-orientation in the origin of lagging chromosomes in human primary cells. J. Cell Sci. 115, 507-515.
11. Cimini, D., Howell, B., Maddox, P., Khodjakov, A., Degrassi, F. and Salmon, E. D. (2001). Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153, 517-527.
12. Cimini, D., Tanzarella, C. and Degrassi, F. (1999). Differences in malsegregation rates obtained by scoring ana-telophases or binucleate cells. Mutagenesis 14, 563-568.
13. Compton, D. A. and Cleveland, D. W. (1994). NuMA, a nuclear protein involved in mitosis and nuclear reformation. Curr. Opin. Cell Biol. 6, 343-346.
14. De Brabander, M., Geuens, G., de Mey, J. and Joniau, M. (1981). Nucleated assembly of mitotic microtubules in living PTK2 cells after release from nocodazole treatment. Cell Motil. 1, 469-483.
15. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
16. Ford, J. H., Schultz, C. J. and Correll, A. T. (1988). Chromosome elimination in micronuclei: a common cause of hypoploidy. Am. J. Hum. Genet. 43, 733-740.
17. Funabiki, H. and Murray, A. W. (2000). The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 102, 411-424.
18. Heneen, W. K. (1975). Kinetochores and microtubules in multipolar mitosis and chromosome orientation. Exp. Cell Res. 91, 57-62.
19. 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.
20. Inoue, S. and Salmon, E. D. (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol. Biol. Cell 6, 1619-1640.
21. Izzo, M., Antoccia, A., Degrassi, F. and Tanzarella, C. (1998). Immunofluorescence analysis of diazepam-induced mitotic apparatus anomalies and chromosome loss in Chinese hamster cells. Mutagenesis 13, 445-451.
22. Kaitna, S., Mendoza, M., Jantsch-Plunger, V. and Glotzer, M. (2000). Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr. Biol. 10, 1172-1181.
23. Khodjakov, A., Cole, R. W., McEwen, B. F., Buttle, K. F. and Rieder, C. L. (1997). Chromosome fragments possessing only one kinetochore can congress to the spindle equator. J. Cell Biol. 136, 229-240.
24. Khodjakov, A., Copenagle, L., Gordon, M. B., Compton, D. A. and Kapoor, T. M. (2003). Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J. Cell Biol. 160, 671-683.
25. King, J. M. and Nicklas, R. B. (2000). Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J. Cell Sci. 113, 3815-3823.
26. Ladrach, K. S. and LaFountain, J. R., Jr (1986). Malorientation and abnormal segregation of chromosomes during recovery from colcemid and nocodazole. Cell Motil. Cytoskeleton 6, 419-427.
27. Levesque, A. A. and Compton, D. A. (2001). The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J. Cell Biol. 154, 1135-1146.
28. Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L. and Mitchison, T. J. (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974.
29. McEwen, B. F., Heagle, A. B., Cassels, G. O., Bottle, K. F. and Rieder, C. L. (1997). Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J. Cell Biol. 137, 1567-1580.
30. Minissi, S., Gustavino, B., Degrassi, F., Tanzarella, C. and Rizzoni, M. (1999). Effect of cytochalasin B on the induction of chromosome missegregation by colchicine at low concentrations in human lymphocytes. Mutagenesis 14, 43-49.
31. Nicklas, R. B. (1971). Mitosis. Adv. Cell Biol. 2, 225-297.
32. Nicklas, R. B. (1983). Measurements of the force produced by the mitotic spindle in anaphase. J. Cell Biol. 97, 542-548.
33. Nicklas, R. B. (1997). How cells get the right chromosomes. Science 275, 632-637.
34. Nicklas, R. B. and Ward, S. C. (1994). Elements of error correction in mitosis: microtubule capture, release, and tension. J. Cell Biol. 126, 1241-1253.
35. Rieder, C. L. (1982). The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int. Rev. Cytol. 79, 1-58.
36. Rieder, C. L. and Hard, R. (1990). Newt lung epithelial cells: cultivation, use, and advantages for biomedical research. Int. Rev. Cytol. 122, 153-220.
37. Rieder, C. L. and Salmon, E. D. (1998). The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol. 8, 310-318.
38. Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. and Goldberg, A. L. (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
39. Roos, U. P. (1973). Light and electron microscopy of rat kangaroo cells in mitosis. II. Kinetochore structure and function. Chromosoma 41, 195-220.
40. Roos, U. P. (1976). Light and electron microscopy of rat kangaroo cells in mitosis. III. Patterns of chromosome behavior during prometaphase. Chromosoma 54, 363-385.
41. Salmon, E. D., Shaw, S. L., Waters, J., Waterman-Storer, C. M., Maddox, P. S., Yeh, E. and Bloom, K. (1998). A high-resolution multimode digital microscope system. Methods Cell Biol. 56, 185-215.
42. Shah, J. V. and Cleveland, D. W. (2000). Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell 103, 997-1000.
43. Shannon, K. B. and Salmon, E. D. (2002). Chromosome dynamics: new light on Aurora B kinase function. Curr. Biol. 12, R458-R460.
44. Shelden, E. and Wadsworth, P. (1996). Stimulation of microtubule dynamic turnover in living cells treated with okadaic acid. Cell Motil. Cytoskeleton 35, 24-34.
45. 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.
46. Stern, B. M. (2002). Mitosis: aurora gives chromosomes a healthy stretch. Curr. Biol. 12, R316-R318.
47. Tanaka, T. U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M. J. and Nasmyth, K. (2002). Evidence that the Ipl1-Slil5 (Aurora kinase-INCENT) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329.
48. Topper, L. M., Bastians, H., Ruderman, J. V. and Gorbsky, G. J. (2001). Elevating the level of Cdc34/Ubc3 ubiquitin-conjugating enzyme in mitosis inhibits association of CENP-E with kinetochores and blocks the metaphase alignment of chromosomes. J. Cell Biol. 154, 707-717.
49. Tousson, A., Zeng, C., Brinkley, B. R. and Valdivia, M. M. (1991). Centrophilin: a novel mitotic spindle protein involved in microtubule nucleation. J. Cell Biol. 112, 427-440.
50. Waters, J. C., Chen, R. H., Murray, A. W. and Salmon, E. D. (1998). Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141, 1181-1191.
51. Wise, D. A. (1999). Cytokinesis in cells undergoing mitosis without genome replication. Cell Biol. Int. 23, 813-816.
52. Wise, D. A. and Brinkley, B. R. (1997). Mitosis in cells with unreplicated genomes (MUGs): spindle assembly and behavior of centromere fragments. Cell Motil. Cytoskeleton 36, 291-302.
53. Wittmann, T., Hyman, A. and Desai, A. (2001). The spindle: a dynamic assembly of microtubules and motors. Nat. Cell Biol. 3, E28-E34.
54. Yu, H. G. and Dawe, R. K. (2000). Functional redundancy in the maize meiotic kinetochore. J. Cell Biol. 151, 131-142.
55. Zhai, Y., Kronebusch, P. J. and Borisy, G. G. (1995). Kinetochore microtubule dynamics and the metaphase-anaphase transition. J. Cell Biol. 131, 721-734.