Meiosis-Specific Stable Binding of Augmin to Acentrosomal Spindle Poles Promotes Biased Microtubule Assembly in Oocytes

English version České info

In the oocytes of many animals including humans, the meiotic spindle assembles without centrosomes. It is still unclear how multiple pathways contribute to spindle microtubule assembly, and whether they are regulated differently in mitosis and meiosis. Augmin is a γ-tubulin recruiting complex which “amplifies” spindle microtubules by generating new microtubules along existing ones in mitosis. Here we show that in Drosophila melanogaster oocytes Augmin is dispensable for chromatin-driven assembly of bulk spindle microtubules, but is required for full microtubule assembly near the poles. The level of Augmin accumulated at spindle poles is well correlated with the degree of chromosome congression. Fluorescence recovery after photobleaching shows that Augmin stably associates with the polar regions of the spindle in oocytes, unlike in mitotic cells where it transiently and uniformly associates with the metaphase spindle. This stable association is enhanced by γ-tubulin and the kinesin-14 Ncd. Therefore, we suggest that meiosis-specific regulation of Augmin compensates for the lack of centrosomes in oocytes by actively biasing sites of microtubule generation within the spindle.

Vyšlo v časopise: Meiosis-Specific Stable Binding of Augmin to Acentrosomal Spindle Poles Promotes Biased Microtubule Assembly in Oocytes. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003562
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003562

Souhrn

Zdroje

1. McKimKS, HawleyRS (1995) Chromosomal control of meiotic cell division. Science 270: 1595–1601.

2. KhodjakovA, ColeRW, OakleyBR, RiederCL (2000) Centrosome-independent mitotic spindle formation in vertebrates. Curr Biol 10: 59–67.

3. BastoR, LauJ, VinogradovaT, GardiolA, WoodsCG, et al. (2006) Flies without centrioles. Cell 125: 1375–1386.

4. MeunierS, VernosI (2012) Microtubule assembly during mitosis - from distinct origins to distinct functions? J Cell Sci 125: 2805–2814.

5. MahoneyNM, GoshimaG, DouglassAD, ValeRD (2006) Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol 16: 564–569.

6. GoshimaG, MayerM, ZhangN, StuurmanN, ValeRD (2008) Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 181: 421–429.

7. UeharaR, NozawaRS, TomiokaA, PetryS, ValeRD, et al. (2009) The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc Natl Acad Sci USA 106: 6998–7003.

8. PetryS, GroenAC, IshiharaK, MitchisonTJ, ValeRD (2013) Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2. Cell 152: 768–777.

9. MeirelesAM, FisherKH, ColombiéN, WakefieldJG, OhkuraH (2009) Wac: a new Augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J Cell Biol 184: 777–784.

10. UeharaR, GoshimaG (2010) Functional central spindle assembly requires de novo microtubule generation in the interchromosomal region during anaphase. J Cell Biol 191: 259–267.

11. LawoS, BashkurovM, MullinM, FerreriaMG, KittlerR, et al. (2009) HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity. Curr Biol 19: 816–826.

12. PetryS, PugieuxC, NédélecFJ, ValeRD (2011) Augmin promotes meiotic spindle formation and bipolarity in Xenopus egg extracts. Proc Natl Acad Sci USA 108: 14473–14478.

13. HottaT, KongZ, HoCM, ZengCJ, HorioT, et al. (2012) Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 2: 1494–1509.

14. HoCM, HottaT, KongZ, ZengCJ, SunJ, et al. (2012) Augmin plays a critical role in organizing the spindle and phragmoplast microtubule arrays in Arabidopsis. Plant Cell 23: 2606–2618.

15. NakaokaY, MikiT, FujiokaR, UeharaR, TomiokaA, et al. (2012) An inducible RNA interference system in Physcomitrella patens reveals a dominant role of augmin in phragmoplast microtubule generation. Plant Cell 24: 1478–1493.

16. WainmanA, BusterDW, DuncanT, MetzJ, MaA, et al. (2009) A new Augmin subunit, Msd1, demonstrates the importance of mitotic spindle-templated microtubule nucleation in the absence of functioning centrosomes. Genes Dev 23: 1876–1881.

17. BucciarelliE, PellacaniC, NaimV, PalenaA, GattiM, et al. (2009) Drosophila Dgt6 interacts with Ndc80, Msps/XMAP215, and gamma-tubulin to promote kinetochore-driven MT formation. Curr Biol 19: 1839–1845.

18. ZhuH, FangK, FangG (2009) FAM29A, a target of Plk1 regulation, controls the partitioning of NEDD1 between the mitotic spindle and the centrosomes. J Cell Sci 122: 2750–2759.

19. JohmuraY, SoungNK, ParkJE, YuLR, ZhouM, et al. (2011) Regulation of microtubule-based microtubule nucleation by mammalian polo-like kinase 1. Proc Natl Acad Sci USA 108: 11446–11451.

20. TsaiCY, NgoB, TapadiaA, HsuPH, WuG, et al. (2011) Aurora-A phosphorylates Augmin complex component Hice1 protein at an N-terminal serine/threonine cluster to modulate its microtubule binding activity during spindle assembly. J Biol Chem 286: 30097–30106.

21. HughesJR, MeirelesAM, FisherKH, GarciaA, AntrobusPR, et al. (2008) A microtubule Interactome: complexes with roles in cell cycle and mitosis. PLoS Biol 6: e98.

22. ReschenRF, ColombieN, WheatleyL, DobbelaereJ, St JohnstonD, et al. (2012) Dgp71WD is required for the assembly of the acentrosomal meiosis I spindle, and is not a general targeting factor for the gamma-TuRC. Biology Open 1: 422–429.

23. HughesSE, BeelerJS, SeatA, SlaughterBD, UnruhJR, et al. (2011) Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes. PLoS Genet 7: e1002209.

24. HatsumiM, EndowSA (1992) Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis. J Cell Sci 101: 547–559.

25. RiederCL, SalmonED (1994) Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J Cell Biol 124: 223–233.

26. NicklasRB, WardSC (1994) Elements of error correction in mitosis: microtubule capture, release, and tension. J Cell Biol 126: 1241–153.

27. CaneS, YeAA, Luks-MorganSJ, MarescaTJ (2013) Elevated polar ejection forces stabilize kinetochore-microtubule attachments. J Cell Biol 200: 203–218.

28. McKimKS, HawleyRS (1995) Chromosomal control of meiotic cell division. Science 270: 1595–1601.

29. TheurkaufWE, HawleyRS (1992) Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol 116: 1167–1180.

30. GillilandWD, HughesSF, ViettiDR, HawleyRS (2009) Congression of achiasmate chromosomes to the metaphase plate in Drosophila melanogaster oocytes. Dev Biol 325: 122–128.

31. HughesSE, GillilandWD, CotittaJL, TakeoS, CollinsKA, et al. (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5: e1000348.

32. ZhangP, HawleyRS (1990) The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the nod locus. Genetics 125: 115–127.

33. HealdR, TournebizeR, BlankT, SandaltzopoulosR, BeckerP, et al. (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382: 420–425.

34. Sambrook J., Fritsch E.F., and Maniatis T. (1989). Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press

35. Harlow E, Lane D (1988) Antibodies: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.

36. Ashburner M, Golic KG, Hawley RS (2005) Drosophila: a laboratory handbook. New York: Cold Spring Harbor Laboratory Press.

37. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. New York: Academic Press.

38. DrysdaleRA, CrosbyMA (2005) The FlyBase Consortium (2005) FlyBase: genes and gene models. Nuc Acids Res 33: D390–D395.

39. CullenCF, OhkuraH (2001) Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3: 637–642.

40. ColombiéN, CullenCF, BrittleAL, JangJK, EarnshawWC, et al. (2008) Dual roles of Incenp crucial to the assembly of the acentrosomal metaphase spindle in female meiosis. Development 135: 3239–3246.