Laser microsurgery provides evidence for merotelic kinetochore attachments in fission yeast cells lacking Pcs1 or Clr4

Cell Cycle

Volumn 9, Issue 19, 2010, Pages 3997-4004

  Rumpf, Cornelia ^a   Cipak, Lubos ^a   Schleiffer, Alexander ^b   Pidoux, Alison ^c   Mechtler, Karl ^b   Tolić Nørrelykke, Iva M ^d   Gregan, Juraj ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Chromosome segregation; Fission yeast; Kinetochore; Merotely; Mitosis

Indexed keywords

CYCLIN DEPENDENT KINASE 1; PCS 1 PROTEIN; PROTEIN; PROTEIN MDE 4; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL MUTANT; CELL STRUCTURE; CENTROMERE; ENZYME ACTIVITY; LASER SURGERY; METAPHASE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SPINDLE CELL; YEAST CELL;

MAMMALIA; SCHIZOSACCHAROMYCETACEAE;

EID: 77958506747     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.19.13233     Document Type: Article

References (72)

1. Biggins S, Walczak CE. Captivating capture: how microtubules attach to kinetochores. Curr Biol 2003; 13:449-60.
2. Santaguida S, Musacchio A. The life and miracles of kinetochores. EMBO J 2009; 28:2511-31.
3. Westermann S, Drubin DG, Barnes G. Structures and functions of yeast kinetochore complexes. Annu Rev Biochem 2007; 76:563-91.
4. Cimini D. Merotelic kinetochore orientation, aneuploidy and cancer. Biochim Biophys Acta 2008; 1786:32-40.
5. Cimini D. Detection and correction of merotelic kinetochore orientation by Aurora B and its partners. Cell Cycle 2007; 6:1558-64. (Pubitemid 47327940)
6. Cimini D, Moree B, Canman JC, Salmon ED. Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J Cell Sci 2003; 116:4213-25.
7. Cimini D, Cameron LA, Salmon ED. Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr Biol 2004; 14:2149-55.
8. Cimini D, Fioravanti D, Salmon ED, Degrassi F. Merotelic kinetochore orientation versus chromosome mono-orientation in the origin of lagging chromosomes in human primary cells. J Cell Sci 2002; 115:507-15. (Pubitemid 34182978)
9. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 2001; 153:517-27.
10. Torosantucci L, Puzzonia Mde S, Cenciarelli C, Rens W, Degrassi F. Aneuploidy in mitosis of PtK1 cells is generated by random loss and nondisjunction of individual chromosomes. J Cell Sci 2009; 122:3455-61.
11. Silkworth WT, Nardi IK, Scholl LM, Cimini D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome missegregation in cancer cells. PLoS One 2009; 4:6564.
12. Bakhoum SF, Thompson SL, Manning AL, Compton DA. Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat Cell Biol 2009; 11:27-35.
13. Thompson SL, Compton DA. Examining the link between chromosomal instability and aneuploidy in human cells. J Cell Biol 2008; 180:665-72.
14. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009; 460:278-82.
15. Martinez AC, van Wely KH. Are aneuploidy and chromosome breakage caused by a CINgle mechanism? Cell Cycle 2010; 9:2275-80.
16. Gregan J, Riedel CG, Pidoux AL, Katou Y, Rumpf C, Schleiffer A, et al. The kinetochore proteins Pcs1 and Mde4 and heterochromatin are required to prevent merotelic orientation. Curr Biol 2007; 17:1190-200. (Pubitemid 47043439)
17. Rabitsch KP, Petronczki M, Javerzat JP, Genier S, Chwalla B, Schleiffer A, et al. Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev Cell 2003; 4:535-48. (Pubitemid 36437560)
18. Khodjakov A, Cole RW, McEwen BF, Buttle KF, Rieder CL. Chromosome fragments possessing only one kinetochore can congress to the spindle equator. J Cell Biol 1997; 136:229-40. (Pubitemid 27063077)
19. Pidoux AL, Uzawa S, Perry PE, Cande WZ, Allshire RC. Live analysis of lagging chromosomes during anaphase and their effect on spindle elongation rate in fission yeast. J Cell Sci 2000; 113:4177-91. (Pubitemid 32000685)
20. Tolic-Norrelykke IM, Sacconi L, Thon G, Pavone FS. Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr Biol 2004; 14:1181-6. (Pubitemid 38893981)
21. Khodjakov A, La Terra S, Chang F. Laser microsurgery in fission yeast; role of the mitotic spindle midzone in anaphase B. Curr Biol 2004; 14:1330-40. (Pubitemid 39081634)
22. Sacconi L, Tolic-Norrelykke IM, Antolini R, Pavone FS. Combined intracellular three-dimensional imaging and selective nanosurgery by a nonlinear microscope. J Biomed Opt 2005; 10:14002.
23. Maghelli N, Tolic-Norrelykke IM. Versatile laser-based cell manipulator. J Biophotonics 2008; 1:299-309.
24. Courtheoux T, Gay G, Gachet Y, Tournier S. Ase1/Prc1-dependent spindle elongation corrects merotely during anaphase in fission yeast. J Cell Biol 2009; 187:399-412.
25. Loncarek J, Kisurina-Evgenieva O, Vinogradova T, Hergert P, La Terra S, Kapoor TM, et al. The centromere geometry essential for keeping mitosis error free is controlled by spindle forces. Nature 2007; 450:745-9. (Pubitemid 350207690)
26. Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, et al. Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 2008; 10:42-52.
27. Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T. Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 2009; 184:383-90.
28. Maresca TJ, Salmon ED. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J Cell Biol 2009; 184:373-81.
29. Wan X, O'Quinn RP, Pierce HL, Joglekar AP, Gall WE, DeLuca JG, et al. Protein architecture of the human kinetochore microtubule attachment site. Cell 2009; 137:672-84.
30. Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 2004; 14:287-301. (Pubitemid 38300206)
31. Kearsey SE, Brimage L, Namdar M, Ralph E, Yang X. In situ assay for analyzing the chromatin binding of proteins in fission yeast. Methods Mol Biol 2005; 296:181-8.
32. Toda T, Umesono K, Hirata A, Yanagida M. Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe. J Mol Biol 1983; 168:251-70.
33. Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 2004; 427:510-7. (Pubitemid 38209104)
34. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 1999; 17:1030-2. (Pubitemid 29474865)
35. Jin QW, Ray S, Choi SH, McCollum D. The nucleolar Net1/Cfi1-related protein Dnt1 antagonizes the septation initiation network in fission yeast. Mol Biol Cell 2007; 18:2924-34. (Pubitemid 47235300)
36. Broadley SA, Hartl FU. The role of molecular chaperones in human misfolding diseases. FEBS Lett 2009; 583:2647-53.
37. Choi SH, Peli-Gulli MP, McLeod I, Sarkeshik A, Yates JR, 3rd, Simanis V, et al. Phosphorylation state defines discrete roles for monopolin in chromosome attachment and spindle elongation. Curr Biol 2009; 19:985-95.
38. Wilson-Grady JT, Villen J, Gygi SP. Phosphoproteome analysis of fission yeast. J Proteome Res 2008; 7:1088-97.
39. Beltrao P, Trinidad JC, Fiedler D, Roguev A, Lim WA, Shokat KM, et al. Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. PLoS Biol 2009; 7:1000134.
40. Gregan J, Zhang C, Rumpf C, Cipak L, Li Z, Uluocak P, et al. Construction of conditional analog-sensitive kinase alleles in the fission yeast Schizosaccharomyces pombe. Nat Protoc 2007; 2:2996-3000.
41. Dischinger S, Krapp A, Xie L, Paulson JR, Simanis V. Chemical genetic analysis of the regulatory role of Cdc2p in the S. pombe septation initiation network. J Cell Sci 2008; 121:843-53. (Pubitemid 351578120)
42. Huang J, Brito IL, Villen J, Gygi SP, Amon A, Moazed D. Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 2006; 20:2887-901. (Pubitemid 44771749)
43. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, et al. Targets of the cyclin-dependent kinase Cdk1. Nature 2003; 425:859-64.
44. Khmelinskii A, Schiebel E. Chromosome segregation: monopolin goes spindle. Curr Biol 2009; 19:482-4.
45. Woodbury EL, Morgan DO. Cdk and APC activities limit the spindle-stabilizing function of Fin1 to anaphase. Nat Cell Biol 2007; 9:106-12.
46. Pereira G, Schiebel E. Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 2003; 302:2120-4. (Pubitemid 38017944)
47. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, et al. The Pfam protein families database. Nucleic Acids Res 2008; 36:281-8.
48. Janke C, Ortiz J, Lechner J, Shevchenko A, Shevchenko A, Magiera MM, et al. The budding yeast proteins Spc24p and Spc25p interact with Ndc80p and Nuf2p at the kinetochore and are important for kinetochore clustering and checkpoint control. EMBO J 2001; 20:777-91. (Pubitemid 32167642)
49. Wigge PA, Kilmartin JV. The Ndc80p complex from Saccharomyces cerevisiae contains conserved centromere components and has a function in chromosome segregation. J Cell Biol 2001; 152:349-60.
50. McCleland ML, Kallio MJ, Barrett-Wilt GA, Kestner CA, Shabanowitz J, Hunt DF, et al. The vertebrate Ndc80 complex contains Spc24 and Spc25 homologs, which are required to establish and maintain kinetochore-microtubule attachment. Curr Biol 2004; 14:131-7. (Pubitemid 38203926)
51. Asakawa H, Hayashi A, Haraguchi T, Hiraoka Y. Dissociation of the Nuf2-Ndc80 complex releases centromeres from the spindle-pole body during meiotic prophase in fission yeast. Mol Biol Cell 2005; 16:2325-38. (Pubitemid 40632215)
52. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 2006; 127:969-82.
53. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 2006; 127:983-97. (Pubitemid 44792248)
54. Ciferri C, Pasqualato S, Screpanti E, Varetti G, Santaguida S, Dos Reis G, et al. Implications for kinetochore- microtubule attachment from the structure of an engineered Ndc80 complex. Cell 2008; 133:427-39. (Pubitemid 351622013)
55. Wei RR, Schnell JR, Larsen NA, Sorger PK, Chou JJ, Harrison SC. Structure of a central component of the yeast kinetochore: the Spc24p/Spc25p globular domain. Structure 2006; 14:1003-9.
56. Kwon MS, Hori T, Okada M, Fukagawa T. CENP-C is involved in chromosome segregation, mitotic checkpoint function and kinetochore assembly. Mol Biol Cell 2007; 18:2155-68. (Pubitemid 46911367)
57. Tanaka K, Chang HL, Kagami A, Watanabe Y. CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev Cell 2009; 17:334-43.
58. Liu ST, Rattner JB, Jablonski SA, Yen TJ. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J Cell Biol 2006; 175:41-53.
59. Nousiainen M, Sillje HH, Sauer G, Nigg EA, Korner R. Phosphoproteome analysis of the human mitotic spindle. Proc Natl Acad Sci USA 2006; 103:5391-6.
60. Raabe I, Vogel SK, Peychl J, Tolic-Norrelykke IM. Intracellular nanosurgery and cell enucleation using a picosecond laser. J Microsc 2009; 234:1-8.
61. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 2006; 441:53-61.
62. Gregan J, Rumpf C, Li Z, Cipak L. What makes centromeric cohesion resistant to separase cleavage during meiosis I but not during meiosis II? Cell Cycle 2008; 7:10-2.
63. Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, Riedel CG, et al. Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 2010; 9:2657-62.
64. Rumpf C, Cipak L, Novatchkova M, Li Z, Polakova S, Dudas A, et al. High-throughput knockout screen in Schizosaccharomyces pombe identifies a novel gene required for efficient homolog disjunction during meiosis I. Cell Cycle 2010; 9:1802-8.
65. Gregan J, Rabitsch PK, Rumpf C, Novatchkova M, Schleiffer A, Nasmyth K. High-throughput knockout screen in fission yeast. Nat Protoc 2006; 1:2457-64.
66. Cipak L, Spirek M, Novatchkova M, Chen Z, Rumpf C, Lugmayr W, et al. An improved strategy for tandem affinity purification-tagging of Schizosaccharomyces pombe genes. Proteomics 2009; 9:4825-8.
67. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 2006; 441:53-61.
68. Gregan J, Riedel CG, Petronczki M, Cipak L, Rumpf C, Poser I, et al. Tandem affinity purification of functional TAP-tagged proteins from human cells. Nat Protoc 2007; 2:1145-51. (Pubitemid 46901293)
69. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389-402. (Pubitemid 27359211)
70. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000; 302:205-17.
71. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007; 35:61-5. (Pubitemid 46056171)
72. Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, Jones DT. Protein structure prediction servers at University College London. Nucleic Acids Res 2005; 33:36-8.