Nsk1 ensures accurate chromosome segregation by promoting association of kinetochores to spindle poles during anaphase B

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4486-4502

  Buttrick, Graham J ^a   Meadows, John C ^a   Lancaster, Theresa C ^a   Vanoosthuyse, Vincent ^b,c   Shepperd, Lindsey A ^a   Hoe, Kwang Lae ^d   Kim, Dong Uk ^d   Park, Han Oh ^e   Hardwick, Kevin G ^b   Millar, Jonathan B A ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITÉ DE LYON   (France)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^e Bioneer Corporation   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; PHOSPHATASE; PROTEIN; PROTEIN NSK1; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CENTROMERE; CHROMOSOME SEGREGATION; DEPHOSPHORYLATION; INTERPHASE; MICROTUBULE ASSEMBLY; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SISTER CHROMATID;

ANAPHASE; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; DYNEINS; KINETOCHORES; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 82655189986     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-07-0608     Document Type: Article

References (62)

1. Akiyoshi B, Nelson CR, Ranish JA, Biggins S (2009). Quantitative proteomic analysis of purified yeast kinetochores identifies a PP1 regulatory subunit. Genes Dev 23, 2887-2899.
2. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A III, Steever AB, Wach A, Philippsen P, Pringle JR (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951. (Pubitemid 28328000)
3. Beauregard PB, Guerin R, Turcotte C, Lindquist S, Rokeach LA (2009). A nucleolar protein allows viability in the absence of the essential ER-residing molecular chaperone calnexin. J Cell Sci 122, 1342-1351.
4. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW (1999). The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13, 532-544. (Pubitemid 29131878)
5. Bohnert KA, Chen JS, Clifford DM, Vander Kooi CW, Gould KL (2009). A link between aurora kinase and Clp1/Cdc14 regulation uncovered by the identification of a fission yeast borealin-like protein. Mol Biol Cell 20, 3646-3659.
6. Cheeseman IM, Anderson S, Jwa M, Green EM, Kang J, Yates JR III, Chan CS, Drubin DG, Barnes G (2002). Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172. (Pubitemid 35292437)
7. Chen CT, Feoktistova A, Chen JS, Shim YS, Clifford DM, Gould KL, McCollum D (2008). The SIN kinase Sid2 regulates cytoplasmic retention of the S. pombe Cdc14-like phosphatase Clp1. Curr Biol 18, 1594-1599.
8. Civelekoglu-Scholey G, Scholey JM (2010). Mitotic force generators and chromosome segregation. Cell Mol Life Sci 67, 2231-2250.
9. Courtheoux T, Gay G, Gachet Y, Tournier S (2009). Ase1/Prc1-dependent spindle elongation corrects merotely during anaphase in fission yeast. J Cell Biol 187, 399-412.
10. Ding R, West RR, Morphew DM, Oakley BR, McIntosh JR (1997). The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol Biol Cell 8, 1461-1479. (Pubitemid 27385570)
11. Franco A, Meadows JC, Millar JB (2007). The Dam1/DASH complex is required for the retrieval of unclustered kinetochores in fission yeast. J Cell Sci 120, 3345-3351. (Pubitemid 350028342)
12. Funabiki H, Hagan I, Uzawa S, Yanagida M (1993). Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol 121, 961-976. (Pubitemid 23154258)
13. Gachet Y, Reyes C, Courtheoux T, Goldstone S, Gay G, Serrurier C, Tournier S (2008). Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2. Mol Biol Cell 19, 1646-1662. (Pubitemid 351805117)
14. Grishchuk EL, McIntosh JR (2006). Microtubule depolymerization can drive poleward chromosome motion in fission yeast. EMBO J 25, 4888-4896. (Pubitemid 44607033)
15. Hagan IM, Hyams JS (1988). The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe. J Cell Sci 89, 343-357.
16. Higuchi T, Uhlmann F (2005). Stabilization of microtubule dynamics at anaphase onset promotes chromosome segregation. Nature 433, 171-176.
17. Hiraoka Y, Toda T, Yanagida M (1984). The NDA3 gene of fission yeast encodes β-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39, 349-358. (Pubitemid 15191218)
18. Holland AJ, Cleveland DW (2009). Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 10, 478-487.
19. Jia Z, Barford D, Flint AJ, Tonks NK (1995). Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268, 1754-1758.
20. Jin Q, Trelles-Sticken E, Scherthan H, Loidl J (1998). Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141, 21-29. (Pubitemid 28182638)
21. Jin QW, Fuchs J, Loidl J (2000). Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113, 1903-1912. (Pubitemid 30386494)
22. Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008). Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181, 587-594. (Pubitemid 351717506)
23. Khodjakov A, La Terra S, Chang F (2004). Laser microsurgery in fission yeast; role of the mitotic spindle midzone in anaphase B. Curr Biol 14, 1330-1340. (Pubitemid 39081634)
24. King MC, Drivas TG, Blobel G (2008). A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134, 427-438.
25. Kitamura E, Tanaka K, Kitamura Y, Tanaka TU (2007). Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21, 3319-3330. (Pubitemid 350277758)
26. Koch A, Krug K, Pengelley S, Macek B, Hauf S (2011). Mulitple substrates of the mitotic kinase Aurora with roles in chromatin regulation identified through quantitative phosphoproteomics of fission yeast. Sci Signal 4, rs6.
27. Krapp A, Schmidt S, Cano E, Simanis V (2001). S. pombe cdc11p, together with sid4p, provides an anchor for septation initiation network proteins on the spindle pole body. Curr Biol 11, 1559-1568. (Pubitemid 32978520)
28. Krawchuk MD, Wahls WP (1999). High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast 15, 1419-1427. (Pubitemid 29445815)
29. Liu D, Vleugel M, Backer CB, Hori T, Fukagawa T, Cheeseman IM, Lampson MA (2010). Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Biol 188, 809-820.
30. Mallavarapu A, Sawin K, Mitchison T (1999). A switch in microtubule dynamics at the onset of anaphase B in the mitotic spindle of Schizosaccharomyces pombe. Curr Biol 9, 1423-1426.
31. Manning AL, Bakhoum SF, Maffini S, Correia-Melo C, Maiato H, Compton DA (2010). CLASP1, astrin and Kif2b form a molecular switch that regulates kinetochore-microtubule dynamics to promote mitotic progression and fidelity. EMBO J 29, 3531-3543.
32. Matsuyama A, Shirai A, Yoshida M (2008). A novel series of vectors for chromosomal integration in fission yeast. Biochem Biophys Res Commun 374, 315-319.
33. Meadows JC, Millar J (2008). Latrunculin A delays anaphase onset in fission yeast by disrupting an Ase1-independent pathway controlling mitotic spindle stability. Mol Biol Cell 19, 3713-3723.
34. Meadows JC, Shepperd LA, Vanoosthuyse V, Lancaster TC, Sochaj AM, Buttrick GJ, Hardwick KG, Millar JBA (2011). Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin 8 motors. Dev Cell 20, 739-750.
35. Miki F, Okazaki K, Shimanuki M, Yamamoto A, Hiraoka Y, Niwa O (2002). The 14-kDa dynein light chain-family protein Dlc1 is required for regular oscillatory nuclear movement and efficient recombination during meiotic prophase in fission yeast. Mol Biol Cell 13, 930-946. (Pubitemid 34250356)
36. Minshull J, Straight A, Rudner AD, Dernburg AF, Belmont A, Murray AW (1996). Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr Biol 6, 1609-1620. (Pubitemid 27050228)
37. Moreno S, Klar A, Nurse P (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194, 795-823.
38. Nabeshima K, Nakagawa T, Straight AF, Murray A, Chikashige Y, Yamashita YM, Hiraoka Y, Yanagida M (1998). Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol Biol Cell 9, 3211-3225. (Pubitemid 28516632)
39. Niwa O, Matsumoto T, Chikashige Y, Yanagida M (1989). Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere. EMBO J 8, 3045-3052. (Pubitemid 19275007)
40. Ohkura H, Kinoshita N, Miyatani S, Toda T, Yanagida M (1989). The fission yeast dis2+ gene required for chromosome disjoining encodes one of two putative type 1 protein phosphatases. Cell 57, 997-1007. (Pubitemid 19168380)
41. Oliferenko S, Balasubramanian MK (2002). Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4, 816-820. (Pubitemid 35214777)
42. Pinsky BA, Kotwaliwale CV, Tatsutani SY, Breed CA, Biggins S (2006). Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol Cell Biol 26, 2648-2660.
43. Pinsky BA, Nelson CR, Biggins S (2009). Protein phosphatase 1 regulates exit from the spindle checkpoint in budding yeast. Curr Biol 19, 1182-1187.
44. Rhind N et al. (2011). Comparative functional genomics of the fission yeasts. Science 332, 930-936.
45. Rieder CL, Alexander SP (1990). Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells. J Cell Biol 110, 81-95.
46. Roguev A, Wiren M, Weissman JS, Krogan NJ (2007). High-throughput genetic interaction mapping in the fission yeast Schizosaccharomyces pombe. Nat Methods 4, 861-866. (Pubitemid 350055586)
47. Rosenberg JS, Cross FR, Funabiki H (2011). KNL1/Spc105 recruits PP1 to silence the spindle assembly checkpoint. Curr Biol 21, 942-947.
48. Sato M, Vardy L, Angel Garcia M, Koonrugsa N, Toda T (2004). Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol Biol Cell 15, 1609-1622. (Pubitemid 38401812)
49. Schmidt JC, Kiyomitsu T, Hori T, Backer CB, Fukagawa T, Cheeseman IM (2010). Aurora B kinase controls the targeting of the Astrin-SKAP complex to bioriented kinetochores. J Cell Biol 191, 269-280.
50. Tanaka K, Kitamura E, Kitamura Y, Tanaka TU (2007). Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J Cell Biol 178, 269-281. (Pubitemid 47076463)
51. Tanaka K, Mukae N, Dewar H, van Breugel M, James EK, Prescott AR, Antony C, Tanaka TU (2005). Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434, 987-994. (Pubitemid 40586041)
52. Tanaka TU (2010). Kinetochore-microtubule interactions: steps towards biorientation. EMBO J 29, 4070-4082.
53. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K (2002). Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329. (Pubitemid 34178397)
54. Thein KH, Kleylein-Sohn J, Nigg EA, Gruneberg U (2007). Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity. J Cell Biol 178, 345-354. (Pubitemid 47196144)
55. Toya M, Sato M, Haselmann U, Asakawa K, Brunner D, Antony C, Toda T (2007). γ-tubulin complex-mediated anchoring of spindle microtubules to spindle-pole bodies requires Msd1 in fission yeast. Nat Cell Biol 9, 646-653. (Pubitemid 47214726)
56. Trautmann S, Rajagopalan S, McCollum D (2004). The S. pombe Cdc14-like phosphatase Clp1p regulates chromosome biorientation and interacts with Aurora kinase. Dev Cell 7, 755-762. (Pubitemid 39462695)
57. Vanoosthuyse V, Hardwick KG (2009). A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr Biol 19, 1176-1181.
58. Vanoosthuyse V, Meadows JC, van der Sar SJ, Millar JB, Hardwick KG (2009). Bub3p facilitates spindle checkpoint silencing in fission yeast. Mol Biol Cell 20, 5096-5105.
59. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A (1998). The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2, 709-718. (Pubitemid 128378979)
60. Woodbury EL, Morgan DO (2007). Cdk and APC activities limit the spindle-stabilizing function of Fin1 to anaphase. Nat Cell Biol 9, 106-112. (Pubitemid 46024204)
61. Yang Y et al. (2008). Phosphorylation of HsMis13 by Aurora B kinase is essential for assembly of functional kinetochore. J Biol Chem 283, 26726-26736.
62. Zhai Y, Kronebusch PJ, Borisy GG (1995). Kinetochore microtubule dynamics and the metaphase-anaphase transition. J Cell Biol 131, 721-734.