Synergy between Multiple Microtubule-Generating Pathways Confers Robustness to Centrosome-Driven Mitotic Spindle Formation

Developmental Cell

Volumn 28, Issue 1, 2014, Pages 81-93

  Hayward, Daniel ^a   Metz, Jeremy ^a   Pellacani, Claudia ^b   Wakefield, JamesG ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b Pasteur Institute   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL GROWTH; CELL NUCLEUS MEMBRANE; CENTROMERE; CENTROSOME; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOSOL; DROSOPHILA; EMBRYO; INTERPHASE; METAPHASE; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CENTROMERE; DROSOPHILA; DROSOPHILA PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; SPINDLE APPARATUS;

EID: 84892443919     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.12.001     Document Type: Article

References (39)

1. Basto R., Scaerou F., Mische S., Wojcik E., Lefebvre C., Gomes R., Hays T., Karess R. Invivo dynamics of the rough deal checkpoint protein during Drosophila mitosis. Curr. Biol. 2004, 14:56-61.
2. Bieling P., Laan L., Schek H., Munteanu E.L., Sandblad L., Dogterom M., Brunner D., Surrey T. Reconstitution of a microtubule plus-end tracking system invitro. Nature 2007, 450:1100-1105.
3. Brunet S., Polanski Z., Verlhac M.H., Kubiak J.Z., Maro B. Bipolar meiotic spindle formation without chromatin. Curr. Biol. 1998, 8:1231-1234.
4. Brust-Mascher I., Civelekoglu-Scholey G., Kwon M., Mogilner A., Scholey J.M. Model for anaphase B: role of three mitotic motors in a switch from poleward flux to spindle elongation. Proc. Natl. Acad. Sci. USA 2004, 101:15938-15943.
5. Brust-Mascher I., Sommi P., Cheerambathur D.K., Scholey J.M. Kinesin-5-dependent poleward flux and spindle length control in Drosophila embryo mitosis. Mol. Biol. Cell 2009, 20:1749-1762.
6. Bucciarelli E., Pellacani C., Naim V., Palena A., Gatti M., Somma M.P. Drosophila Dgt6 interacts with Ndc80, Msps/XMAP215, and gamma-tubulin to promote kinetochore-driven MT formation. Curr. Biol. 2009, 19:1839-1845.
7. Cesario J., McKim K.S. RanGTP is required for meiotic spindle organization and the initiation of embryonic development in Drosophila. J.Cell Sci. 2011, 124:3797-3810.
8. Colombié N., Głuszek A.A., Meireles A.M., Ohkura H. Meiosis-specific stable binding of augmin to acentrosomal spindle poles promotes biased microtubule assembly in oocytes. PLoS Genet. 2013, 9:e1003562.
9. Conduit P.T., Brunk K., Dobbelaere J., Dix C.I., Lucas E.P., Raff J.W. Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr. Biol. 2010, 20:2178-2186.
10. Goshima G. Identification of a TPX2-like microtubule-associated protein in Drosophila. PLoS ONE 2011, 6:e28120.
11. Goshima G., Wollman R., Goodwin S.S., Zhang N., Scholey J.M., Vale R.D., Stuurman N. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316:417-421.
12. Goshima G., Mayer M., Zhang N., Stuurman N., Vale R.D. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J.Cell Biol. 2008, 181:421-429.
13. Hallen M.A., Ho J., Yankel C.D., Endow S.A. Fluorescence recovery kinetic analysis of gamma-tubulin binding to the mitotic spindle. Biophys. J. 2008, 95:3048-3058.
14. Heald R., Tournebize R., Blank T., Sandaltzopoulos R., Becker P., Hyman A., Karsenti E. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 1996, 382:420-425.
15. Heald R., Tournebize R., Habermann A., Karsenti E., Hyman A. Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J.Cell Biol. 1997, 138:615-628.
16. Hughes S.E., Beeler J.S., Seat A., Slaughter B.D., Unruh J.R., Bauerly E., Matthies H.J., Hawley R.S. Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes. PLoS Genet. 2011, 7:e1002209.
17. Inoue S. Effect of temperature on the birefringence of the mitotic spindle. Biol. Bull. 1952, 103:316.
18. Inoue S. Organisation and function of the mitotic spindle. Ann. N Y Acad. Sci. 1964, 90:529.
19. Jang J.K., Rahman T., Kober V.S., Cesario J., McKim K.S. Misregulation of the kinesin-like protein Subito induces meiotic spindle formation in the absence of chromosomes and centrosomes. Genetics 2007, 177:267-280.
20. Koffa M.D., Casanova C.M., Santarella R., Köcher T., Wilm M., Mattaj I.W. HURP is part of a Ran-dependent complex involved in spindle formation. Curr. Biol. 2006, 16:743-754.
21. Khodjakov A., Cole R.W., Oakley B.R., Rieder C.L. Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 2000, 10:59-67.
22. Liang Z.-Y., Hallen M.A., Endow S.A. Mature Drosophila meiosis I spindles comprise microtubules of mixed polarity. Curr. Biol. 2009, 19:163-168.
23. Lucas E.P., Raff J.W. Maintaining the proper connection between the centrioles and the pericentriolar matrix requires Drosophila centrosomin. J.Cell Biol. 2007, 178:725-732.
24. Mahoney N.M., Goshima G., Douglass A.D., Vale R.D. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr. Biol. 2006, 16:564-569.
25. Maiato H., Rieder C.L., Khodjakov A. Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J.Cell Biol. 2004, 167:831-840.
26. Megraw T.L., Kao L.R., Kaufman T.C. Zygotic development without functional mitotic centrosomes. Curr. Biol. 2001, 11:116-120.
27. Moutinho-Pereira S., Debec A., Maiato H. Microtubule cytoskeleton remodeling by acentriolar microtubule-organizing centers at the entry and exit from mitosis in Drosophila somatic cells. Mol. Biol. Cell 2009, 20:2796-2808.
28. Petry S., Groen A.C., Ishihara K., Mitchison T.J., Vale R.D. Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2. Cell 2013, 152:768-777.
29. Radford S.J., Jang J.K., McKim K.S. The chromosomal passenger complex is required for meiotic acentrosomal spindle assembly and chromosome biorientation. Genetics 2012, 192:417-429.
30. Schuh M., Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 2007, 130:484-498.
31. Shimamoto Y., Maeda Y.T., Ishiwata S., Libchaber A.J., Kapoor T.M. Insights into the micromechanical properties of the metaphase spindle. Cell 2011, 145:1062-1074.
32. Silljé H.H.W., Nagel S., Körner R., Nigg E.A. HURP is a Ran-importin beta-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes. Curr. Biol. 2006, 16:731-742.
33. Tan S., Lyulcheva E., Dean J., Bennett D. Mars promotes dTACC dephosphorylation on mitotic spindles to ensure spindle stability. J.Cell Biol. 2008, 182:27-33.
34. Torosantucci L., De Luca M., Guarguaglini G., Lavia P., Degrassi F. Localized RanGTP accumulation promotes microtubule nucleation at kinetochores in somatic mammalian cells. Mol. Biol. Cell 2008, 19:1873-1882.
35. Uehara R., Nozawa R.S., Tomioka A., Petry S., Vale R.D., Obuse C., Goshima G. The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 2009, 106:6998-7003.
36. Wainman A., Buster D.W., Duncan T., Metz J., Ma A., Sharp D., Wakefield J.G. A new Augmin subunit, Msd1, demonstrates the importance of mitotic spindle-templated microtubule nucleation in the absence of functioning centrosomes. Genes Dev. 2009, 23:1876-1881.
37. Walker R.A., O'Brien E.T., Pryer N.K., Soboeiro M.F., Voter W.A., Erickson H.P., Salmon E.D. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J.Cell Biol. 1988, 107:1437-1448.
38. Wu C., Singaram V., McKim K.S. mei-38 is required for chromosome segregation during meiosis in Drosophila females. Genetics 2008, 180:61-72.
39. Zhang G., Breuer M., Förster A., Egger-Adam D., Wodarz A. Mars, a Drosophila protein related to vertebrate HURP, is required for the attachment of centrosomes to the mitotic spindle during syncytial nuclear divisions. J.Cell Sci. 2009, 122:535-545.