The relative roles of centrosomal and kinetochore-driven microtubules in Drosophila spindle formation

Experimental Cell Research

Volumn 318, Issue 12, 2012, Pages 1375-1380

  Gatti, Maurizio ^a   Bucciarelli, Elisabetta ^a   Lattao, Ramona ^a   Pellacani, Claudia ^a   Mottier Pavie, Violaine ^a   Giansanti, Maria Grazia ^a   Somma, Maria Patrizia ^a   Bonaccorsi, Silvia ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Centrosomes; Drosophila; Kinetochores; Male meiosis; Microtubule growth; Mitosis; Spindle assembly

Indexed keywords

GAMMA TUBULIN;

BRAIN CELL; CENTRIOLE; CENTROMERE; CENTROSOME; CHROMOSOME; CHROMOSOME SEGREGATION; DROSOPHILA MELANOGASTER; LARVA; MEIOSIS; METAPHASE; MICROTUBULE; MITOSIS; MUTANT; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN POLYMERIZATION; REVIEW; SOMATIC CELL; SPERMATOCYTE; SPERMATOGENESIS; SPINDLE CELL;

EID: 84861920619     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.05.001     Document Type: Review

References (40)

1. O'Connell C.B., Khodjakov A.L. Cooperative mechanisms of mitotic spindle formation. J. Cell Sci. 2007, 120:1717-1722.
2. Walczak C.E., Heald R. Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 2008, 265:111-158.
3. Duncan T., Wakefield J.G. 50 ways to build a spindle: the complexity of microtubule generation during mitosis. Chromosome Res. 2011, 19:321-333.
4. Luders J., Stearns T. Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 2007, 8:161-167.
5. Bettencourt-Dias M., Glover D.M. Centrosome biogenesis and function: centrosomics brings new understanding. Nat. Rev. Mol. Cell Biol. 2007, 8:451-463.
6. Bonaccorsi S., Giansanti M.G., Gatti M. Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nat. Cell Biol. 2000, 2:54-56.
7. Giansanti M.G., Gatti M., Bonaccorsi S. The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 2001, 128:1137-1145.
8. Megraw T.L., Kao L.R., Kaufman T.C. Zygotic development without functional mitotic centrosomes. Curr. Biol. 2001, 11:116-120.
9. Basto R., Lau J., Vinogradova T., Gardiol A., Woods C.G., Khodjakov A., Raff J.W. Flies without centrioles. Cell 2006, 125:1375-1386.
10. Varmark H., Llamazares S., Rebollo E., Lange B., Reina J., Schwarz H., Gonzalez C. Asterless is a centriolar protein required for centrosome function and embryo development in Drosophila. Curr. Biol. 2007, 17:1735-1745.
11. Blachon S., Gopalakrishnan J., Omori Y., Polyanovsky A., Church A., Nicastro D., Malicki J., Avidor-Reiss T. Drosophila asterless and vertebrate Cep152 are orthologs essential for centriole duplication. Genetics 2008, 180:2081-2094.
12. Giansanti M.G., Bucciarelli E., Bonaccorsi S., Gatti M. Drosophila SPD-2 is an essential centriole component required for PCM recruitment and astral-microtubule nucleation. Curr. Biol. 2008, 18:303-309.
13. Debec A., Szollosi A., Szollosi D. A Drosophila melanogaster cell line lacking centriole. Biol. Cell 1982, 44:133-138.
14. Debec A., Detraves C., Montmory C., Geraud G., Wright M. Polar organization of gamma-tubulin in acentriolar mitotic spindles of Drosophila melanogaster cells. J. Cell Sci. 1995, 108(Pt 7):2645-2653.
15. 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.
16. 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.
17. Rieder C.L. Kinetochore fiber formation in animal somatic cells: dueling mechanisms come to a draw. Chromosoma 2005, 114:310-318.
18. O'Connell C.B., Loncarek J., Kalab P., Khodjakov A. Relative contributions of chromatin and kinetochores to mitotic spindle assembly. J. Cell Biol. 2009, 187:43-51.
19. 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.
20. 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.
21. Mottier-Pavie V., Cenci G., Verni F., Gatti M., Bonaccorsi S. Phenotypic analysis of misato function reveals roles of noncentrosomal microtubules in Drosophila spindle formation. J. Cell Sci. 2011, 124:706-717.
22. 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.
23. 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.
24. Hughes J.R., Meireles A.M., Fisher K.H., Garcia A., Antrobus P.R., Wainman A., Zitzmann N., Deane C., Ohkura H., Wakefield J.G. A microtubule interactome: complexes with roles in cell cycle and mitosis. PLoS Biol. 2008, 6:e98.
25. Meireles A.M., Fisher K.H., Colombie N., Wakefield J.G., Ohkura H. Wac: a new augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J. Cell Biol. 2009, 184:777-784.
26. 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.
27. Somma M.P., Ceprani F., Bucciarelli E., Naim V., De Arcangelis V., Piergentili R., Palena A., Ciapponi L., Giansanti M.G., Pellacani C., Petrucci R., Cenci G., Verni F., Fasulo B., Goldberg M.L., Di Cunto F., Gatti M. Identification of Drosophila mitotic genes by combining co-expression analysis and RNA interference. PLoS Genet. 2008, 4:e1000126.
28. Toso A., Winter J.R., Garrod A.J., Amaro A.C., Meraldi P., McAinsh A.D. Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J. Cell Biol. 2009, 184:365-372.
29. Karess R. Rod-Zw10-Zwilch: a key player in the spindle checkpoint. Trends Cell Biol. 2005, 15:386-392.
30. Lattao R., Bonaccorsi S., Gatti M. Giant meiotic spindles in males from Drosophila species with giant sperm tails. J. Cell Sci. 2012, 125:584-588.
31. Gonzalez C., Tavosanis G., Mollinari C. Centrosomes and microtubule organisation during Drosophila development. J. Cell Sci. 1998, 111(Pt 18):2697-2706.
32. Baker J.D., Adhikarakunnathu S., Kernan M.J. Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 2004, 131:3411-3422.
33. Bonaccorsi S., Giansanti M.G., Gatti M. Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J. Cell Biol. 1998, 142:751-761.
34. Bucciarelli E., Giansanti M.G., Bonaccorsi S., Gatti M. Spindle assembly and cytokinesis in the absence of chromosomes during Drosophila male meiosis. J. Cell Biol. 2003, 160:993-999.
35. Williams B., Leung G., Maiato H., Wong A., Li Z., Williams E.V., Kirkpatrick C., Aquadro C.F., Rieder C.L., Goldberg M.L. Mitch - a rapidly evolving component of the Ndc80 kinetochore complex required for correct chromosome segregation in Drosophila. J. Cell Sci. 2007, 120:3522-3533.
36. Khodjakov A., Cole R.W., Oakley B.R., Rieder C.L. Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 2000, 10:59-67.
37. Garrett S., Auer K., Compton D.A., Kapoor T.M. hTPX2 is required for normal spindle morphology and centrosome integrity during vertebrate cell division. Curr. Biol. 2002, 12:2055-2059.
38. Gruss O.J., Wittmann M., Yokoyama H., Pepperkok R., Kufer T., Sillje H., Karsenti E., Mattaj I.W., Vernos I. Chromosome-induced microtubule assembly mediated by TPX2 is required for spindle formation in HeLa cells. Nat. Cell Biol. 2002, 4:871-879.
39. Tulu U.S., Fagerstrom C., Ferenz N.P., Wadsworth P. Molecular requirements for kinetochore-associated microtubule formation in mammalian cells. Curr. Biol. 2006, 16:536-541.
40. Bird A.W., Hyman A.A. Building a spindle of the correct length in human cells requires the interaction between TPX2 and Aurora A. J. Cell. Biol. 2008, 182:289-300.