The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo

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Microtubule-microfilament interactions are important for cytokinesis and subcellular localization of proteins and mRNAs. In the early zebrafish embryo, astral microtubule-microfilament interactions also facilitate a stereotypic segregation pattern of germ plasm ribonucleoparticles (GP RNPs), which is critical for their eventual selective inheritance by germ cells. The precise mechanisms and molecular mediators for both cytoskeletal interactions and GP RNPs segregation are the focus of intense research. Here, we report the molecular identification of a zebrafish maternal-effect mutation motley as Birc5b, a homolog of the mammalian Chromosomal Passenger Complex (CPC) component Survivin. The meiosis and mitosis defects in motley/birc5b mutant embryos are consistent with failed CPC function, and additional defects in astral microtubule remodeling contribute to failures in the initiation of cytokinesis furrow ingression. Unexpectedly, the motley/birc5b mutation also disrupts cortical microfilaments and GP RNP aggregation during early cell divisions. Birc5b localizes to the tips of astral microtubules along with polymerizing cortical F-actin and the GP RNPs. Mutant Birc5b co-localizes with cortical F-actin and GP RNPs, but fails to associate with astral microtubule tips, leading to disorganized microfilaments and GP RNP aggregation defects. Thus, maternal Birc5b localizes to astral microtubule tips and associates with cortical F-actin and GP RNPs, potentially linking the two cytoskeletons to mediate microtubule-microfilament reorganization and GP RNP aggregation during early embryonic cell cycles in zebrafish. In addition to the known mitotic function of CPC components, our analyses reveal a non-canonical role for an evolutionarily conserved CPC protein in microfilament reorganization and germ plasm aggregation.

Vyšlo v časopise: The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003448
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003448

Souhrn

Zdroje

1. von DassowG (2009) Concurrent cues for cytokinetic furrow induction in animal cells. Trends Cell Biol 19: 165–173.

2. RuchaudS, CarmenaM, EarnshawWC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798–812.

3. CarmenaM (2008) Cytokinesis: the final stop for the chromosomal passengers. Biochem Soc Trans 36: 367–370.

4. EarnshawWC, CookeCA (1991) Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation. J Cell Sci 98: 443–461.

5. FraserAG, JamesC, EvanGI, HengartnerMO (1999) Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr Biol 9: 292–301.

6. KaitnaS, MendozaM, Jantsch-PlungerV, GlotzerM (2000) Incenp and an Aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr Biol 10: 1172–1181.

7. AdamsRR, MaiatoH, EarnshawWC, CarmenaM (2001) Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and choromosome segregation. J Cell Biol 153: 865–880.

8. HondaR, KornerR, NiggEA (2003) Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14: 3325–3341.

9. TeradaY, TatsukaM, SuzukiF, YasudaY, FujitaW, et al. (1998) AIM-1: a mammalian midbody-associated protein required for cytokinesis. EMBO J 17: 667–676.

10. HümmerS, MayerTU (2009) Cdk1 negatively regulates midzone localization of the mitotic kinesin MKlp2 and the chromosomal passenger complex. Curr Biol 19: 607–612.

11. Szafer-GlusmanE, FullerMT, GiansantiMG (2011) Role of Survivin in cytokinesis revealed by a separation-of-function allele. Mol Biol Cell 22: 3779–3790.

12. ExtavourCG, AkamM (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130: 5869–5884.

13. LantzVA, ClemensSE, MillerKG (1999) The actin cytoskeleton is required for maintenance of posterior pole plasm components in the Drosophila embryo. Mech Devel 85: 111–122.

14. ZimyaninVL, BelayaK, PecreauxJ, GilchristMJ, ClarkA, et al. (2008) In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134: 843–853.

15. LeritDA, GavisER (2011) Transport of germ plasm on astral microtubules directs germ cell development in Drosophila. Curr Biol 21: 439–448.

16. TheuschEV, BrownKJ, PelegriF (2006) Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Dev Biol 292: 129–141.

17. Pelegri F, Mullins M (2011) Genetic screens for mutations affecting adult traits and parental-effect genes. In: Detrich HWI, Westerfield M, Zon LI, editors. Methods Cell Biol. pp. 83–120.

18. DelvaeyeM, De VrieseA, ZwertsF, BetzI, MoonsM, et al. (2009) Role of the 2 zebrafish survivin genes in vasculo-angiogenesis, neurogenesis, cardiogenesis and hematopoiesis. BMC Dev Biol 9: 25.

19. SunSC, WeiL, LiM, LinSL, XuBZ, et al. (2009) Perturbation of survivin expression affects chromosome alignment and spindle checkpoint in mouse oocyte meiotic maturation. Cell Cycle 8: 3365–3372.

20. WangK, JiangG-J, WeiL, LiangX-W, MiaoD-Q, et al. (2011) Survivin is a critical regulator of spindle organization and chromosome segregation during rat oocyte meiotic maturation. Zygote 19: 307–313.

21. YabeT, GeX, LindemanR, NairS, RunkeG, et al. (2009) The maternal-effect gene cellular island encodes Aurora B kinase and is essential for furrow formation in the early zebrafish embryo. PLoS Genet 5: e1000518 doi:10.1371/journal.pgen.1000518.

22. YoonC, KawakamiK, HopkinsN (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124: 3157–3165.

23. BraatAK, ZandbergenT, van de WaterS, GoosHJT, ZivkovicD (1999) Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dyn 216: 153–167.

24. PelegriF, KnautH, MaischeinH-M, Schulte-MerkerS, Nüsslein-VolhardC (1999) A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr Biol 9: 1431–1440.

25. LindemanR, PelegriF (2010) Vertebrate maternal-effect genes: insights into fertilization, early cleavage divisions, and germ cell determinant localization from studies in the zebrafish. Mol Rep Dev 77: 299–313.

26. AmbrosiniG, AdidaC, AltieriDC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Medicine 3: 917–921.

27. BirnbaumMJ, ClemRJ, MillerLK (1994) An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 68: 2521–2528.

28. VerhagenAM, CoulsonEJ, VauxDL (2001) Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2: REVIEWS3009.

29. CaoL, WangZ, YangX, XieL, YuL (2008) The evolution of BIR domain and its containing proteins. FEBS letters 582: 3817–3822.

30. AltieriDC (2006) The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr Opin Cell Biol 18: 609–615.

31. MaAC, LinR, ChanPK, LeungJC, ChanLY, et al. (2007) The role of survivin in angiogenesis during zebrafish embryonic development. BMC Dev Biol 7: 50.

32. MaAC, ChungMI, LiangR, LeungAY (2009) The role of survivin2 in primitive hematopoiesis during zebrafish development. Leukemia 23: 712–720.

33. KaitnaS, PasierbekP, JantschM, LoidlJ, GlotzerM (2002) The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homolgous chromosomes during meiosis. Curr Biol 12: 798–812.

34. SampathSC, OhiR, LeismannO, SalicA, PozniakovskiA, et al. (2004) The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell 118: 187–202.

35. GaoS, BiansantiMG, ButtrickG, RamasubramanyanS, AutonA, et al. (2008) Australin: a chromosomal passenger protein required specifically for Drosophila melanogaster male meiosis. J Cell Biol 180: 521–535.

36. CourtoisA, SchuhM, EllenbergJ, HiiragiT (2012) The transition form meiotic to mitotic spindle assembly is gradual during early mammalian development. J Cell Biol 198: 357–370.

37. CaoL, YanX, WuY, HuH, QL, et al. (2006) Survivin mutant (Surv-DD70, 71AA) disrupts the interaction of Survivin with Aurora B and causes multinucleation in HeLa cells. Biochem Biophys Res Commun 346: 400–407.

38. LensSM, RodriguezJA, VaderG, SpanSW, GiacconeG, et al. (2006) Uncoupling the central spindle-associated function of the chromosomal passenger complex from its role at centromeres. Mol Biol Cell 17: 1897–1909.

39. YueZ, CarvalhoA, XuZ, YuanX, CardinaleS, et al. (2008) Deconstructing Survivin: comprehensive genetic analysis of Survivin function by conditional knockout in a vertebrate cell line. J Cell Biol 183: 279–296.

40. KellyAE, GhenoiuC, XueJZ, ZierhutC, KimuraH, et al. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235–239.

41. WangF, DaiJ, DaumJR, NiedzialkowskaE, BanerjeeB, et al. (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora at centromers in mitosis. Science 330: 231–235.

42. YamagishiY, HondaT, TannoY, WatanabeY (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330: 239–243.

43. KnautH, PelegriF, BohmannK, SchwarzH, Nüsslein-VolhardC (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically prior to germ line specification. J Cell Biol 149: 875–888.

44. DekensMPS, PelegriFJ, MaischeinH-M, Nüsslein-VolhardC (2003) The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebrafish zygote. Development 130: 3907–3916.

45. YabeT, GeX, PelegriF (2007) The zebrafish maternal-effect gene cellular atoll encodes the centriolar component Sas-6 and defects in its paternal function promote whole genome duplication. Dev Biol 312: 44–60.

46. LindemanRE, PelegriF (2012) Localized products of futile cycle/lrmp promote centrosome-nucleus attachment in the zebrafish zygote. Curr Biol 22: 843–851.

47. DechantR, GlotzerM (2003) Centrosome separation and central spindle assembly act in reduncant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev Cell 4: 333–344.

48. López de HerediaM, JansenR-P (2004) mRNA localization and the cytoskeleton. Curr Opin Cell Biol 16: 80–85.

49. RobbDL, HeasmanJ, RaatsJ, WylieC (1996) A kinesin-like protein is required for germ plasm aggregation in Xenopus. Cell 87: 823–831.

50. KosakaK, KawakamiK, SakamotoH, InoueK (2007) Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech Dev 124: 279–289.

51. SekiS, KouyaT, TsuchiyaR, ValdezDM, JinB, et al. (2008) Development of a reliable in vitro maturation system for zebrafish oocytes. Reproduction 135: 285–292.

52. NairS, LindemanRE, PelegriF (2013) In vitro oocyte culture-based manipulation of zebrafish maternal genes. Dev Dyn 242: 44–52.

53. KaneDA, KimmelCB (1993) The zebrafish midblastula transition. Development 119: 447–456.

54. OlivierN, Luengo-OrozMA, DuloquinL, FaureE, SavyT, et al. (2010) Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science 329: 967–971.

55. FieldCM, WührM, AndersonGA, KuehHY, SticklandD, et al. (2011) Actin behavior in bulk cytoplasm is cell cycle regulated in early vertebrate embryos. J Cell Sci 124: 2086–2095.

56. WührM, TanES, ParkerSK, DetrichHWIII, MitchinsonTJ (2010) A model for cleavage plane determination in early amphibian and fish embryos. Curr Biol 20: 2040–2045.