Abscission Is Regulated by the ESCRT-III Protein Shrub in Germline Stem Cells
Abscission is the final step of cytokinesis which allows the physical separation of sister cells through the scission of a thin cytoplasmic bridge that links them at the end of mitosis. The duration of abscission varies depending on cell types, indicating that the event is developmentally regulated. Recently, we have identified two kinases, Aurora B and CycB/Cdk-1, which regulate the timing of abscission in germ cells and in mammalian cells. However, these kinases are upstream regulators and do not perform abscission per se. Here, we show that Shrub, a potential target of Aurora B and one of the most downstream effectors of abscission, is required for complete abscission in germline stem cells. In the absence of Shrub, the mother stem cell remains linked to its daughter cells, which then share the same cytoplasm and cannot differentiate. Loss of Shrub and Aurora B have opposite effects on abscission duration suggesting that Aurora B regulates negatively Shrub. We further show that Shrub acts together with its interactor Lethal giant disc to ensure proper abscission timing.
Vyšlo v časopise:
Abscission Is Regulated by the ESCRT-III Protein Shrub in Germline Stem Cells. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004653
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004653
Souhrn
Abscission is the final step of cytokinesis which allows the physical separation of sister cells through the scission of a thin cytoplasmic bridge that links them at the end of mitosis. The duration of abscission varies depending on cell types, indicating that the event is developmentally regulated. Recently, we have identified two kinases, Aurora B and CycB/Cdk-1, which regulate the timing of abscission in germ cells and in mammalian cells. However, these kinases are upstream regulators and do not perform abscission per se. Here, we show that Shrub, a potential target of Aurora B and one of the most downstream effectors of abscission, is required for complete abscission in germline stem cells. In the absence of Shrub, the mother stem cell remains linked to its daughter cells, which then share the same cytoplasm and cannot differentiate. Loss of Shrub and Aurora B have opposite effects on abscission duration suggesting that Aurora B regulates negatively Shrub. We further show that Shrub acts together with its interactor Lethal giant disc to ensure proper abscission timing.
Zdroje
1. Agromayor M, Martin-Serrano J (2013) Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol 23: 433–441. doi: 10.1016/j.tcb.2013.04.006 23706391
2. Sanger JM, Pochapin MB, Sanger JW (1985) Midbody sealing after cytokinesis in embryos of the sea urchin Arabacia punctulata. Cell Tissue Res 240: 287–292. 3995553
3. Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9: 257–262. 10370240
4. Mullins JM, Biesele JJ (1977) Terminal phase of cytokinesis in D-98s cells. J Cell Biol 73: 672–684. 873994
5. Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J (2011) Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A 108: 4846–4851. doi: 10.1073/pnas.1102714108 21383202
6. Guizetti J, Schermelleh L, Mantler J, Maar S, Poser I, et al. (2011) Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 331: 1616–1620. doi: 10.1126/science.1201847 21310966
7. Schiel JA, Park K, Morphew MK, Reid E, Hoenger A, et al. (2011) Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci 124: 1411–1424. doi: 10.1242/jcs.081448 21486954
8. Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, et al. (2011) Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13: 981–988. doi: 10.1038/ncb2279 21706022
9. Fededa JP, Gerlich DW (2012) Molecular control of animal cell cytokinesis. Nat Cell Biol 14: 440–447. doi: 10.1038/ncb2482 22552143
10. Bastos RN, Barr FA (2010) Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J Cell Biol 191: 751–760. doi: 10.1083/jcb.201008108 21079244
11. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, et al. (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26: 4215–4227. doi: 10.1038/sj.emboj.7601850 17853893
12. Lee HH, Elia N, Ghirlando R, Lippincott-Schwartz J, Hurley JH (2008) Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 322: 576–580. doi: 10.1126/science.1162042 18948538
13. Carlton JG, Martin-Serrano J (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316: 1908–1912. 17556548
14. Iwamori T, Iwamori N, Ma L, Edson MA, Greenbaum MP, et al. (2010) TEX14 interacts with CEP55 to block cell abscission. Mol Cell Biol 30: 2280–2292. doi: 10.1128/MCB.01392-09 20176808
15. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, et al. (2006) The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125: 85–98. 16615892
16. Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, et al. (2009) Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136: 473–484. doi: 10.1016/j.cell.2008.12.020 19203582
17. Carlton JG, Caballe A, Agromayor M, Kloc M, Martin-Serrano J (2012) ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336: 220–225. doi: 10.1126/science.1217180 22422861
18. Capalbo L, Montembault E, Takeda T, Bassi ZI, Glover DM, et al. (2012) The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis. Open Biol 2: 120070. doi: 10.1098/rsob.120070 22724069
19. Thoresen SB, Campsteijn C, Vietri M, Schink KO, Liestol K, et al. (2014) ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nat Cell Biol 16: 550–560. doi: 10.1038/ncb2959 24814515
20. Mathieu J, Cauvin C, Moch C, Radford SJ, Sampaio P, et al. (2013) Aurora B and cyclin B have opposite effects on the timing of cytokinesis abscission in Drosophila germ cells and in vertebrate somatic cells. Dev Cell 26: 250–265. doi: 10.1016/j.devcel.2013.07.005 23948252
21. Huynh JR, St Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14: R438–449. 15182695
22. de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125: 2781–2789. 9655801
23. Snapp EL, Iida T, Frescas D, Lippincott-Schwartz J, Lilly MA (2004) The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 15: 4512–4521. doi: 10.1091/mbc.E04-06-0475 15292454
24. Jagut M, Mihaila-Bodart L, Molla-Herman A, Alin MF, Lepesant JA, et al. (2013) A mosaic genetic screen for genes involved in the early steps of Drosophila oogenesis. G3 (Bethesda) 3: 409–425. doi: 10.1534/g3.112.004747 23450845
25. Chen D, Wang Q, Huang H, Xia L, Jiang X, et al. (2009) Effete-mediated degradation of Cyclin A is essential for the maintenance of germline stem cells in Drosophila. Development 136: 4133–4142. doi: 10.1242/dev.039032 19906849
26. Hawkins NC, Thorpe J, Schupbach T (1996) Encore, a gene required for the regulation of germ line mitosis and oocyte differentiation during Drosophila oogenesis. Development 122: 281–290. 8565840
27. Lilly MA, Spradling AC (1996) The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 10: 2514–2526. 8843202
28. Van Buskirk C, Schupbach T (2002) Half pint regulates alternative splice site selection in Drosophila. Dev Cell 2: 343–353. 11879639
29. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407. doi: 10.1038/nmeth.1592 21460824
30. McKearin D, Ohlstein B (1995) A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121: 2937–2947. 7555720
31. Song X, Wong MD, Kawase E, Xi R, Ding BC, et al. (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131: 1353–1364. 14973291
32. Gilboa L, Lehmann R (2004) Repression of primordial germ cell differentiation parallels germ line stem cell maintenance. Curr Biol 14: 981–986. 15182671
33. Ables ET, Drummond-Barbosa D (2013) Cyclin E controls Drosophila female germline stem cell maintenance independently of its role in proliferation by modulating responsiveness to niche signals. Development 140: 530–540. doi: 10.1242/dev.088583 23293285
34. Salzmann V, Chen C, Chiang CY, Tiyaboonchai A, Mayer M, et al. (2014) Centrosome-dependent asymmetric inheritance of the midbody ring in Drosophila germline stem cell division. Mol Biol Cell 25: 267–275. doi: 10.1091/mbc.E13-09-0541 24227883
35. Troost T, Jaeckel S, Ohlenhard N, Klein T (2012) The tumour suppressor Lethal (2) giant discs is required for the function of the ESCRT-III component Shrub/CHMP4. J Cell Sci 125: 763–776. doi: 10.1242/jcs.097261 22389409
36. Martinelli N, Hartlieb B, Usami Y, Sabin C, Dordor A, et al. (2012) CC2D1A is a regulator of ESCRT-III CHMP4B. J Mol Biol 419: 75–88. doi: 10.1016/j.jmb.2012.02.044 22406677
37. Morita E, Colf LA, Karren MA, Sandrin V, Rodesch CK, et al. (2010) Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc Natl Acad Sci U S A 107: 12889–12894. doi: 10.1073/pnas.1005938107 20616062
38. Childress JL, Acar M, Tao C, Halder G (2006) Lethal giant discs, a novel C2-domain protein, restricts notch activation during endocytosis. Curr Biol 16: 2228–2233. doi: 10.1016/j.cub.2006.09.031 17088062
39. Jaekel R, Klein T (2006) The Drosophila Notch inhibitor and tumor suppressor gene lethal (2) giant discs encodes a conserved regulator of endosomal trafficking. Dev Cell 11: 655–669. 17084358
40. Gallagher CM, Knoblich JA (2006) The conserved c2 domain protein lethal (2) giant discs regulates protein trafficking in Drosophila. Dev Cell 11: 641–653. 17084357
41. Vaccari T, Rusten TE, Menut L, Nezis IP, Brech A, et al. (2009) Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J Cell Sci 122: 2413–2423. doi: 10.1242/jcs.046391 19571114
42. Hanson PI, Roth R, Lin Y, Heuser JE (2008) Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J Cell Biol 180: 389–402. doi: 10.1083/jcb.200707031 18209100
43. Kirilly D, Wong JJ, Lim EK, Wang Y, Zhang H, et al. (2011) Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron 72: 86–100. doi: 10.1016/j.neuron.2011.08.003 21982371
44. Schuh M, Lehner CF, Heidmann S (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17: 237–243. 17222555
45. Karpova N, Bobinnec Y, Fouix S, Huitorel P, Debec A (2006) Jupiter, a new Drosophila protein associated with microtubules. Cell Motil Cytoskeleton 63: 301–312. 16518797
46. Murray MJ, Saint R (2007) Photoactivatable GFP resolves Drosophila mesoderm migration behaviour. Development 134: 3975–3983. 17942486
47. Buratovich MA, Bryant PJ (1997) Enhancement of overgrowth by gene interactions in lethal(2)giant discs imaginal discs from Drosophila melanogaster. Genetics 147: 657–670. 9335602
48. Huynh JR, Shulman JM, Benton R, St Johnston D (2001) PAR-1 is required for the maintenance of oocyte fate in Drosophila. Development 128: 1201–1209. 11245586
49. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. 8223268
50. Van Doren M, Williamson AL, Lehmann R (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8: 243–246. 9501989
51. Chen D, McKearin DM (2003) A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130: 1159–1170. 12571107
52. Chou TB, Perrimon N (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131: 643–653. 1628809
53. Xu T, Rubin GM (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223–1237. 8404527
54. Byers TJ, Dubreuil R, Branton D, Kiehart DP, Goldstein LS (1987) Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J Cell Biol 105: 2103–2110. 2824526
55. Hanyu-Nakamura K, Kobayashi S, Nakamura A (2004) Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development 131: 4545–4553. 15342479
56. Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM (1998) pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev 12: 1483–1494. 9585508
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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