Fission yeast Alp14 is a dose-dependent plus end-tracking microtubule polymerase

Molecular Biology of the Cell

Volumn 23, Issue 15, 2012, Pages 2878-2890

  Al Bassam, Jawdat ^a,b   Kim, Hwajin ^c   Flor Parra, Ignacio ^c   Lal, Neeraj ^a   Velji, Hamida ^b   Chang, Fred ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMODIMER; TUBULIN;

ARTICLE; CONTROLLED STUDY; FUNGAL STRAIN; FUNGUS MUTANT; IN VITRO STUDY; IN VIVO STUDY; INTERPHASE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE; YEAST;

INTERPHASE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MUTATION; PROTEIN BINDING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TUBULIN;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84864759021     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-03-0205     Document Type: Article

References (55)

1. 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.
2. Akhmanova A, Steinmetz MO (2011). Microtubule end binding: EBs sense the guanine nucleotide state. Curr Biol 21, R283-R285.
3. Al-Bassam J, Chang F (2011). Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol 21, 604-614.
4. Al-Bassam J, Kim H, Brouhard G, van Oijen A, Harrison SC, Chang F (2010). CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 19, 245-258.
5. Al-Bassam J, Larsen NA, Hyman AA, Harrison SC (2007). Crystal structure of a TOG domain: conserved features of XMAP215/Dis1-family TOG domains and implications for tubulin binding. Structure 15, 355-362.
6. 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.
7. Basu R, Chang F (2011). Characterization of dip1p reveals a switch in Arp2/3-dependent actin assembly for fission yeast endocytosis. Curr Biol 21, 905-916.
8. 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.
9. Bieling P, Laan L, Schek H, Munteanu EL, Sandblad L, Dogterom M, Brunner D, Surrey T (2007). Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450, 1100-1105.
10. Bratman SV, Chang F (2007). Stabilization of overlapping microtubules by fission yeast CLASP. Dev Cell 13, 812-827.
11. Bratman SV, Chang F (2008). Mechanisms for maintaining microtubule bundles. Trends Cell Biol 18, 580-586.
12. Brittle AL, Ohkura H (2005). Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J 24, 1387-1396.
13. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, Howard J, Hyman AA (2008). XMAP215 is a processive microtubule polymerase. Cell 132, 79-88.
14. Browning H, Hayles J, Mata J, Aveline L, Nurse P, McIntosh JR (2000). Tea2p is a kinesin-like protein required to generate polarized growth in fission yeast. J Cell Biol 151, 15-28.
15. Brunner D, Nurse P (2000). CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102, 695-704.
16. Busch KE, Brunner D (2004). The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr Biol 14, 548-559.
17. 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.
18. Cassimeris L, Morabito J (2004). TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol Biol Cell 15, 1580-1590.
19. Coffman VC, Wu P, Parthun MR, Wu JQ (2011). CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J Cell Biol 195, 563-572.
20. Currie JD, Stewman S, Schimizzi G, Slep KC, Ma A, Rogers SL (2011). The microtubule lattice and plus-end association of Drosophila Mini spindles is spatially regulated to fine-tune microtubule dynamics. Mol Biol Cell 22, 4343-4361.
21. Gandhi SR, Gierlinski M, Mino A, Tanaka K, Kitamura E, Clayton L, Tanaka TU (2011). Kinetochore-dependent microtubule rescue ensures their efficient and sustained interactions in early mitosis. Dev Cell 21, 920-933.
22. 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.
23. 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.
24. Gard DL, Becker BE, Josh Romney S (2004). MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int Rev Cytol 239, 179-272.
25. Gard DL, Kirschner MW (1987). A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105, 2203-2215.
26. Gardner MK, Charlebois BD, Janosi IM, Howard J, Hunt AJ, Odde DJ (2011). Rapid microtubule self-assembly kinetics. Cel 146, 582-592.
27. Grissom PM, Fiedler T, Grishchuk EL, Nicastro D, West RR, McIntosh JR (2009). Kinesin-8 from fission yeast: a heterodimeric, plus-end-directed motor that can couple microtubule depolymerization to cargo movement. Mol Biol Cell 20, 963-972.
28. Honnappa S et al. (2009). An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366-376.
29. Hoog JL, Schwartz C, Noon AT, O'Toole ET, Mastronarde DN, McIntosh JR, Antony C (2007). Organization of interphase microtubules in fission yeast analyzed by electron tomography. Dev Cell 12, 349-361.
30. Hsu KS, Toda T (2011). Ndc80 internal loop interacts with Dis1/TOG to ensure proper kinetochore-spindle attachment in fission yeast. Curr Biol 21, 214-220.
31. Janson ME, Loughlin R, Loiodice I, Fu C, Brunner D, Nedelec FJ, Tran PT (2007). Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128, 357-368.
32. Joglekar AP, Salmon ED, Bloom KS (2008). Counting kinetochore protein numbers in budding yeast using genetically encoded fluorescent proteins. Methods Cell Biol 85, 127-151.
33. Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M (2006). Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712.
34. Maurer SP, Bieling P, Cope J, Hoenger A, Surrey T (2011). GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc Natl Acad Sci USA 108, 3988-3993.
35. Maurer SP, Fourniol FJ, Bohner G, Moores CA, Surrey T (2012). EBs recognize a nucleotide-dependent structural cap at growing microtubule ends. Cell 149, 371-382.
36. Mitchison T, Kirschner M (1984). Dynamic instability of microtubule growth. Nature 312, 237-242.
37. Nabeshima K, Kurooka H, Takeuchi M, Kinoshita K, Nakaseko Y, Yanagida M (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.
38. 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.
39. Roque H, Ward JJ, Murrells L, Brunner D, Antony C (2010). The fission yeast XMAP215 homolog Dis1p is involved in microtubule bundle organization. PLoS One 5, e14201.
40. Sato M, Toda T (2007). Alp7/TACC is a crucial target in Ran-GTPase-dependent spindle formation in fission yeast. Nature 447, 334-337.
41. 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.
42. Sawin KE, Tran PT (2006). Cytoplasmic microtubule organization in fission yeast. Yeast 23, 1001-1014.
43. Schek HT 3rd, Gardner MK, Cheng J, Odde DJ, Hunt AJ (2007). Microtubule assembly dynamics at the nanoscale. Curr Biol 17, 1445-1455.
44. Shirasu-Hiza M, Coughlin P, Mitchison T (2003). Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J Cell Biol 161, 349-358.
45. Sirotkin V, Berro J, Macmillan K, Zhao L, Pollard TD (2011). Quantitative analysis of the mechanism of endocytic actin patch assembly and disassembly in fission yeast. Mol Biol Cell 21, 2894-2904.
46. Slep KC (2010). Structural and mechanistic insights into microtubule end-binding proteins. Curr Opin Cell Biol 22, 88-95.
47. Slep KC, Vale RD (2007). Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol Cell 27, 976-991.
48. Snaith HA, Anders A, Samejima I, Sawin KE (2010). New and old reagents for fluorescent protein tagging of microtubules in fission yeast; experimental and critical evaluation. Methods Cell Biol 97, 147-172.
49. Tournebize R, Popov A, Kinoshita K, Ashford AJ, Rybina S, Pozniakovsky A, Mayer TU, Walczak CE, Karsenti E, Hyman AA (2000). Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2, 13-19.
50. 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.
51. 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.
52. Walker RA, O'Brien ET, Pryer NK, Soboeiro MF, Voter WA, Erickson HP, Salmon ED (1988). Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol 107, 1437-1448.
53. West RR, Malmstrom T, Troxell CL, McIntosh JR (2001). Two related kinesins, klp5+ and klp6+, foster microtubule disassembly and are required for meiosis in fission yeast. Mol Biol Cell 12, 3919-3932.
54. Widlund PO, Stear JH, Pozniakovsky A, Zanic M, Reber S, Brouhard GJ, Hyman AA, Howard J (2011). XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc Natl Acad Sci USA 108, 2741-2746.
55. Wu JQ, Pollard TD (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.