The fission yeast XMAP215 homolog dis1p is involved in microtubule bundle organization

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Roque, Hélio ^a   Ward, Jonathan J ^a   Murrells, Lindsay ^a   Brunner, Damian ^a   Antony, Claude ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN ASE1P; PROTEIN DIS1P; PROTEIN KLP2P; PROTEIN XMAP215; UNCLASSIFIED DRUG; ASE1 PROTEIN, S POMBE; DIS1 PROTEIN, S POMBE; KLP2 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN; XENOPUS PROTEIN; XMAP215 PROTEIN, XENOPUS;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; GENE OVEREXPRESSION; INTERMETHOD COMPARISON; INTERPHASE; MICROSCOPY; MICROTUBULE ASSEMBLY; NONHUMAN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SCHIZOSACCHAROMYCES POMBE; WILD TYPE; YEAST CELL; BIOLOGICAL MODEL; COMPUTER PROGRAM; CONFOCAL MICROSCOPY; CYTOSKELETON; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; METHODOLOGY; MICROTUBULE; SCHIZOSACCHAROMYCES; ULTRASTRUCTURE;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

CYTOSKELETON; INTERPHASE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SOFTWARE; XENOPUS PROTEINS;

EID: 78649921413     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014201     Document Type: Article

References (61)

1. Wittmann T, Hyman A, Desai A (2001) The spindle: a dynamic assembly of microtubules and motors. Nat Cell Biol 3: E28-34.
2. Gordon-Weeks PR (2004) Microtubules and growth cone function. J Neurobiol 58: 70-83.
3. Reinsch S, Gonczy P (1998) Mechanisms of nuclear positioning. J Cell Sci 111(Pt 16): 2283-2295.
4. Tran PT, Marsh L, Doye V, Inoue S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153: 397-411.
5. Karsenti E, Nedelec F, Surrey T (2006) Modelling microtubule patterns. Nat Cell Biol 8: 1204-1211.
6. Hagan IM (1998) The fission yeast microtubule cytoskeleton. J Cell Sci 111(Pt 12): 1603-1612.
7. Hayles J, Nurse P (2001) A journey into space. Nat RevMol Cell Biol 2: 647-656.
8. Sawin KE, Nurse P (1998) Regulation of cell polarity by microtubules in fission yeast. J Cell Biol 142: 457-471.
9. Hoog JL, Schwartz C, Noon AT, O'Toole ET, Mastronarde DN, et al. (2007) Organization of interphase microtubules in fission yeast analyzed by electron tomography. Dev Cell 12: 349-361.
10. Drummond DR, Cross RA (2000) Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr Biol 10: 766-775.
11. Brunner D, Nurse P (2000) CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102: 695-704.
12. Busch KE, Hayles J, Nurse P, Brunner D (2004) Tea2p kinesin is involved in spatial microtubule organization by transporting tip1p on microtubules. Dev Cell 6: 831-843.
13. Sawin KE, Snaith HA (2004) Role of microtubules and tea1p in establishment and maintenance of fission yeast cell polarity. J Cell Sci 117: 689-700.
14. Tran PT, Maddox P, Chang F, Inoue S (1999) Dynamic confocal imaging of interphase and mitotic microtubules in the fission yeast, S. pombe. Biol Bull 197: 262-263.
15. Sawin KE, Lourenco PC, Snaith HA (2004) Microtubule nucleation at nonspindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr Biol 14: 763-775.
16. Venkatram S, Tasto JJ, Feoktistova A, Jennings JL, Link AJ, et al. (2004) Identification and characterization of two novel proteins affecting fission yeast gamma-tubulin complex function. Mol Biol Cell 15: 2287-2301.
17. Venkatram S, Jennings JL, Link A, Gould KL (2005) Mto2p, a novel fission yeast protein required for cytoplasmic microtubule organization and anchoring of the cytokinetic actin ring. Mol Biol Cell 16: 3052-3063.
18. Samejima I, Lourenco PC, Snaith HA, Sawin KE (2005) Fission yeast mto2p regulates microtubule nucleation by the centrosomin-related protein mto1p. Mol Biol Cell 16: 3040-3051.
19. Janson ME, Setty TG, Paoletti A, Tran PT (2005) Efficient formation of bipolar microtubule bundles requires microtubule-bound gamma-tubulin complexes. J Cell Biol 169: 297-308.
20. King MC, Drivas TG, Blobel G (2008) A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134: 427-438.
21. Thadani R, Ling YC, Oliferenko S (2009) The fission yeast TACC protein Mia1p stabilizes microtubule arrays by length-independent crosslinking. Curr Biol 19: 1861-1868.
22. Loiodice I, Staub J, Setty TG, Nguyen NP, Paoletti A, et al. (2005) Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol Biol Cell 16: 1756-1768.
23. Janson ME, Loughlin R, Loiodice I, Fu C, Brunner D, et al. (2007) Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128: 357-368.
24. Troxell CL, Sweezy MA, West RR, Reed KD, Carson BD, et al. (2001) pkl1(+)and klp2(+): Two kinesins of the Kar3 subfamily in fission yeast perform different functions in both mitosis and meiosis. Mol Biol Cell 12: 3476-3488.
25. Braun M, Drummond DR, Cross RA, McAinsh AD (2009) The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATP-dependent sorting mechanism. Nat Cell Biol.
26. Bratman SV, Chang F (2007) Stabilization of overlapping microtubules by fission yeast CLASP. Dev Cell 13: 812-827.
27. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, 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.
28. Foethke D, Makushok T, Brunner D, Nedelec F (2009) Force- and lengthdependent catastrophe activities explain interphase microtubule organization in fission yeast. Mol Syst Biol 5: 241.
29. Tischer C, Brunner D, Dogterom M (2009) Force- and kinesin-8-dependent effects in the spatial regulation of fission yeast microtubule dynamics. Mol Syst Biol 5: 250.
30. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, et al. (2008) XMAP215 is a processive microtubule polymerase. Cell 132: 79-88.
31. Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9: 309-322.
32. Garcia MA, Vardy L, Koonrugsa N, Toda T (2001) Fission yeast ch-TOG/ XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint. Embo J 20: 3389-3401.
33. Nabeshima K, Kurooka H, Takeuchi M, Kinoshita K, Nakaseko Y, et al. (1995) p93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites. Genes Dev 9: 1572-1585.
34. Garcia MA, Koonrugsa N, Toda T (2002) Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast. Embo J 21: 6015-6024.
35. Nakaseko Y, Nabeshima K, Kinoshita K, Yanagida M (1996) Dissection of fission yeast microtubule associating protein p93Dis1: regions implicated in regulated localization and microtubule interaction. Genes Cells 1: 633-644.
36. Aoki K, Nakaseko Y, Kinoshita K, Goshima G, Yanagida M (2006) CDC2 phosphorylation of the fission yeast dis1 ensures accurate chromosome segregation. Curr Biol 16: 1627-1635.
37. Al-Bassam J, van Breugel M, Harrison SC, Hyman A (2006) Stu2p binds tubulin and undergoes an open-to-closed conformational change. J Cell Biol 172: 1009-1022.
38. van Breugel M, Drechsel D, Hyman A (2003) Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-associated proteins is a plus end-binding microtubule destabilizer. J Cell Biol 161: 359-369.
39. McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol 15: 43-51.
40. Hoog JL, Antony C (2007) Whole-cell investigation of microtubule cytoskeleton architecture by electron tomography. Methods Cell Biol 79: 145-167.
41. Yamashita A, Sato M, Fujita A, Yamamoto M, Toda T (2005) The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol Biol Cell 16: 1378-1395.
42. Daga RR, Lee KG, Bratman S, Salas-Pino S, Chang F (2006) Self-organization of microtubule bundles in anucleate fission yeast cells. Nat Cell Biol 8: 1108-1113.
43. Furuta K, Toyoshima YY (2008) Minus-End-Directed Motor Ncd Exhibits Processive Movement that Is Enhanced by Microtubule Bundling In Vitro. Curr Biol 18: 152-157.
44. Sharp DJ, Yu KR, Sisson JC, Sullivan W, Scholey JM (1999) Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat Cell Biol 1: 51-54.
45. Segbert C, Barkus R, Powers J, Strome S, Saxton WM, et al. (2003) KLP-18, a Klp2 kinesin, is required for assembly of acentrosomal meiotic spindles in Caenorhabditis elegans. Mol Biol Cell 14: 4458-4469.
46. Mollinari C, Kleman JP, Jiang W, Schoehn G, Hunter T, et al. (2002) PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol 157: 1175-1186.
47. Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW (1999) The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous crossbridges between microtubules. Proc Natl Acad Sci U S A 96: 14931-14936.
48. Ding R, McDonald KL, McIntosh JR (1993) Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol 120: 141-151.
49. O'Toole ET, Mastronarde DN, Giddings TH, Jr., Winey M, Burke DJ, et al. (1997) Three-dimensional analysis and ultrastructural design of mitotic spindles from the cdc20 mutant of Saccharomyces cerevisiae. Mol Biol Cell 8: 1-11.
50. Winey M, Mamay CL, O'Toole ET, Mastronarde DN, Giddings TH, Jr., et al. (1995) Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J Cell Biol 129: 1601-1615.
51. Unsworth A, Masuda H, Dhut S, Toda T (2008) Fission yeast kinesin-8 Klp5 and Klp6 are interdependent for mitotic nuclear retention and required for proper microtubule dynamics. Mol Biol Cell 19: 5104-5115.
52. O'Toole ET, McDonald KL, Mantler J, McIntosh JR, Hyman AA, et al. (2003) Morphologically distinct microtubule ends in the mitotic centrosome of Caenorhabditis elegans. J Cell Biol 163: 451-456.
53. Carazo-Salas RE, Antony C, Nurse P (2005) The kinesin Klp2 mediates polarization of interphase microtubules in fission yeast. Science 309: 297-300.
54. Hitt AL, Cross AR, Williams RC, Jr. (1990) Microtubule solutions display nematic liquid crystalline structure. J Biol Chem 265: 1639-1647.
55. Nakaseko Y, Goshima G, Morishita J, Yanagida M (2001) M phase-specific kinetochore proteins in fission yeast: microtubule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase. Curr Biol 11: 537-549.
56. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51.
57. Gilbert PF (1972) The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. II. Direct methods. Proc R Soc Lond B Biol Sci 182: 89-102.
58. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120: 343-352.
59. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
60. McDonald KL, O'Toole ET, Mastronarde DN, McIntosh JR (1992) Kinetochore microtubules in PTK cells. J Cell Biol 118: 369-383.
61. Marsh BJ, Mastronarde DN, McIntosh JR, Howell KE (2001) Structural evidence for multiple transport mechanisms through the Golgi in the pancreatic beta-cell line, HIT-T15. Biochem Soc Trans 29: 461-467.