Misorientation and reduced stretching of aligned sister kinetochores promote chromosome missegregation in EB1- or APC-depleted cells

EMBO Journal

Volumn 25, Issue 12, 2006, Pages 2814-2827

  Draviam, V M ^a   Shapiro, I ^a   Aldridge, B ^a   Sorger, P K ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aneuploidy; Chromosome segregation; Kinetochore; Microtubule associated protein

Indexed keywords

APC PROTEIN; BINDING PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN EB1; UNCLASSIFIED DRUG;

ANAPHASE; ANEUPLOIDY; ARTICLE; CARCINOGENESIS; CENTROMERE; CHROMOSOME LOSS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; METAPHASE; MICROSCOPY; MICROTUBULE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SISTER CHROMATID;

ADENOMATOUS POLYPOSIS COLI PROTEIN; CHROMOSOME SEGREGATION; CHROMOSOMES, HUMAN; GENES, DOMINANT; HELA CELLS; HUMANS; KINETOCHORES; METAPHASE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; MUTATION; NONDISJUNCTION, GENETIC; PHENOTYPE;

EID: 33745542004     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601168     Document Type: Article

References (48)

1. Aist JR, Liang H, Berns MW (1993) Astral and spindle forces in PtK2 cells during anaphase B: a laser microbeam study. J Cell Sci 104 (Part 4): 1207-1216
2. Akhmanova A, Hoogenraad CC (2005) Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol 17: 47-54
3. Alter O, Brown PO, Botstein D (2000) Singular value decomposition for genome-wide expression data processing and modeling. Proc Natl Acad Sci USA 97: 10101-10106
4. Asakawa K, Toya M, Sato M, Kanai M, Kume K, Goshima T, Garcia MA, Hirata D, Toda T (2005) MaB, the fission yeast EB1 homologue, cooperates with Bubi spindle checkpoint to prevent monopolar attachment. EMBO Rep 6: 1194-1200
5. Askham JM, Vaughan KT, Goodson HV, Morrison EE (2002) Evidence that an interaction between EB1 and p 150 (Glued) is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol Biol Cell 13: 3627-3645
6. Beinhauer JD, Hagan IM, Hegemann JH, Fleig U (1997) Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form. J Cell Biol 139: 717-728
7. Bienz M (2002) The subcellular destinations of APC proteins. Nat Rev Mol Cell Biol 3: 328-338
8. Bu W, Su LK (2003) Characterization of functional domains of human EB1 family proteins. J Biol Chem 278: 49721-49731
9. Burds AA, Lutum AS, Sorger PK (2005) Generating chromosome instability through the simultaneous deletion of Mad2 and p53. Proc Natl Acad Sci USA 102: 11296-11301
10. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B (1998) Mutations of mitotic checkpoint genes in human cancers. Nature 392: 300-303
11. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED (2001) Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 153: 517-527
12. Draviam VM, Xie S, Sorger PK (2004) Chromosome segregation and genomic stability. Curr Opin Genet Dev 14: 120-125
13. Dujardin D, Wacker UI, Moreau A, Schroer TA, Rickard JE, De Mey JR (1998) Evidence for a role of CLIP-170 in the establishment of metaphase chromosome alignment. J Cell Biol 141: 849-862
14. Echeverri CJ, Paschal BM, Vaughan KT, Vallee RB (1996) Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 132: 617-633
15. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB, Wang Y, Vallee RB (2000) A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat Cell Biol 2: 784-791
16. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, Clevers H (2001) Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 3: 433-438
17. Gergely F, Draviam VM, Raff JW (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17: 336-341
18. Green RA, Kaplan KB (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
19. Green RA, Wollman R, Kaplan KB (2005) APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol Biol Cell 16: 4609-4622
20. Howard J, Hyman AA (2003) Dynamics and mechanics of the microtubule plus end. Nature 422: 753-758
21. Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM, Rieder CL, Salmon ED (2001) Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155: 1159-1172
22. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS (2001) A role for the adenomatous polyposis coli protein in chromosome segregation. Nat Cell Biol 3: 429-432
23. Kapoor TM (2004) Chromosome segregation: correcting improper attachment. Curr Biol 14: R1011-R1013
24. Kelling J, Sullivan K, Wilson L, Jordan MA (2003) Suppression of centromere dynamics by Taxol in living osteosarcoma cells. Cancer Res 63: 2794-2801
25. Kinoshita K, Noetzel TL, Arnal I, Drechsel DN, Hyman AA (2006) Global and local control of microtubule destabilization promoted by a catastrophe kinesin MCAK/XKCM1. J Muscle Res Cell Motil 27: 107-114
26. Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170
27. Lengauer C, Kinzler KW, Vogelstein B (1997) Genetic instability in colorectal cancers. Nature 386: 623-627
28. Lens SM, Medema RH (2003) The survivin/Aurora B complex: its role in coordinating tension and attachment. Cell Cycle 2: 507-510
29. Maiato H, Fairley EA, Rieder CL, Swedlow JR, Sunkel CE, Earnshaw WC (2003) Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 113: 891-904
30. Maiato H, Khodjakov A, Rieder CL (2005) Drosophila CLASP is required for the incorporation of microtubule subunits into fluxing kinetochore fibres. Nat Cell Biol 7: 42-47
31. Maiato H, Rieder CL, Khodjakov A (2004) Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J Cell Biol 167: 831-840
32. Mayer ML, Pot I, Chang M, Xu H, Aneliunas V, Kwok T, Newitt R, Aebersold R, Boone C, Brown GW, Hieter P (2004) Identification of protein complexes required for efficient sister chromatid cohesion. Mol Biol Cell 15: 1736-1745
33. Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7: 45-60
34. Meraldi P, Sorger PK (2005) A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J 24: 1621-1633
35. Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741
36. Pinsky BA, Biggins S (2005) The spindle checkpoint: tension versus attachment. Trends Cell Biol 15: 486-493
37. Rieder CL (1981) The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84: 145-158
38. Rieder CL, Maiato H (2004) Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 7: 637-651
39. Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158: 873-884
40. Sato M, Sekido Y, Horio Y, Takahashi M, Saito H, Minna JD, Shimokata K, Hasegawa Y (2000) Infrequent mutation of the hBUB1 and hBUBR1 genes in human lung cancer. Jpn J Cancer Res 91: 504-509
41. Shelby RD, Hahn KM, Sullivan KF (1996) Dynamic elastic behavior of alpha-satellite DNA domains visualized in situ in living human cells. J Cell Biol 135: 545-557
42. Skibbens RV, Rieder CL, Salmon ED (1995) Kinetochore motility after severing between sister centromeres using laser microsurgery: evidence that kinetochore directional instability and position is regulated by tension. J Cell Sci 108 (Part 7): 2537-2548
43. Spencer F, Gerring SL, Connelly C, Hieter P (1990) Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124: 237-249
44. Suarez-Merino B, Hubank M, Revesz T, Harkness W, Hayward R, Thompson D, Darling JL, Thomas DG, Warr TJ (2005) Microarray analysis of pediatric ependymoma identifies a cluster of 112 candidate genes including four transcripts at 22q12.1-q13.3. Nearo-oncology 7: 20-31
45. Tanenbaum ME, Galjart N, van Vugt MA, Medema RH (2005) CLIP-170 facilitates the formation of kinetochore-microtubule attachments. EMBO J 25: 45-57
46. Tanenbaum ME, Galjart N, van Vugt MA, Medema RH (2006) CLIP-170 facilitates the formation of kinetochore-microtubule attachments. EMBO J 25: 45-57
47. Tirnauer JS, Canman JC, Salmon ED, Mitchison TJ (2002) EB1 targets to kinetochores with attached, polymerizing microtubules. Mol Biol Cell 13: 4308-4316
48. Yamaguchi K, Okami K, Hibi K, Wehage SL, Jen J, Sidransky D (1999) Mutation analysis of hBUB1 in aneuploid HNSCC and lung cancer cell lines. Cancer Lett 139: 183-187