#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

ALIX and ESCRT-III Coordinately Control Cytokinetic Abscission during Germline Stem Cell Division


Cytokinesis, the final step of cell division, concludes with a process termed abscission, during which the two daughter cells physically separate. In spite of their importance, the molecular machineries controlling abscission are poorly characterized especially in the context of living metazoan tissues. Here we provide molecular insight into the mechanism of abscission using the fruit fly Drosophila melanogaster as a model organism. We show that the scaffold protein ALIX and the ESCRT-III component Shrub are required for completion of abscission in Drosophila female germline stem cells (fGSCs). ESCRT-III has been implicated in topologically similar membrane scission events as abscission, namely intraluminal vesicle formation at endosomes and virus budding. Here we demonstrate that ALIX and Shrub co-localize and interact to promote abscission with correct timing in Drosophila fGSCs. We thus show that ALIX and ESCRT-III coordinately control abscission in Drosophila fGSCs cells and report an evolutionarily conserved function of the ALIX/ESCRT-III pathway during cytokinesis in a multi-cellular organism.


Vyšlo v časopise: ALIX and ESCRT-III Coordinately Control Cytokinetic Abscission during Germline Stem Cell Division. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004904
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004904

Souhrn

Cytokinesis, the final step of cell division, concludes with a process termed abscission, during which the two daughter cells physically separate. In spite of their importance, the molecular machineries controlling abscission are poorly characterized especially in the context of living metazoan tissues. Here we provide molecular insight into the mechanism of abscission using the fruit fly Drosophila melanogaster as a model organism. We show that the scaffold protein ALIX and the ESCRT-III component Shrub are required for completion of abscission in Drosophila female germline stem cells (fGSCs). ESCRT-III has been implicated in topologically similar membrane scission events as abscission, namely intraluminal vesicle formation at endosomes and virus budding. Here we demonstrate that ALIX and Shrub co-localize and interact to promote abscission with correct timing in Drosophila fGSCs. We thus show that ALIX and ESCRT-III coordinately control abscission in Drosophila fGSCs cells and report an evolutionarily conserved function of the ALIX/ESCRT-III pathway during cytokinesis in a multi-cellular organism.


Zdroje

1. Glotzer M (2005) The molecular requirements for cytokinesis. Science 307: 1735–1739. doi: 10.1126/science.1096896 15774750

2. Eggert US, Mitchison TJ, Field CM (2006) Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 75: 543–566. doi: 10.1146/annurev.biochem.74.082803.133425 16756502

3. Barr FA, Gruneberg U (2007) Cytokinesis: placing and making the final cut. Cell 131: 847–860. doi: 10.1016/j.cell.2007.11.011 18045532

4. Green RA, Paluch E, Oegema K (2012) Cytokinesis in animal cells. Annu Rev Cell Dev Biol 28: 29–58. doi: 10.1146/annurev-cellbio-101011-155718 22804577

5. Cabernard C (2012) Cytokinesis in Drosophila melanogaster. Cytoskeleton (Hoboken) 69: 791–809. doi: 10.1002/cm.21060

6. D’Avino P (2009) How to scaffold the contractile ring for a safe cytokinesis—lessons from Anillin-related proteins. J Cell Sci 122: 1071–1079. doi: 10.1242/jcs.034785 19339546

7. Fededa JP, Gerlich DW (2012) Molecular control of animal cell cytokinesis. Nat Cell Biol 14: 440–447. doi: 10.1038/ncb2482 22552143

8. Chen CT, Hehnly H, Doxsey SJ (2012) Orchestrating vesicle transport, ESCRTs and kinase surveillance during abscission. Nat Rev Mol Cell Biol 13: 483–488. doi: 10.1038/nrm3395 22781903

9. 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

10. Elia N, Ott C, Lippincott-Schwartz J (2013) Incisive imaging and computation for cellular mysteries: lessons from abscission. Cell 155: 1220–1231. doi: 10.1016/j.cell.2013.11.011 24315094

11. 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

12. Caballe A, Martin-Serrano J (2011) ESCRT machinery and cytokinesis: the road to daughter cell separation. Traffic 12: 1318–1326. doi: 10.1111/j.1600-0854.2011.01244.x 21722282

13. Carlton JG, Agromayor M, Martin-Serrano J (2008) Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci U S A 105: 10541–10546. doi: 10.1073/pnas.0802008105 18641129

14. Carlton JG, Martin-Serrano J (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316: 1908–1912. doi: 10.1126/science.1143422 17556548

15. 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

16. El Amine N, Kechad A, Jananji S, Hickson GR (2013) Opposing actions of septins and Sticky on Anillin promote the transition from contractile to midbody ring. J Cell Biol 203: 487–504. doi: 10.1083/jcb.201305053 24217622

17. Mullins JM, Biesele JJ (1977) Terminal phase of cytokinesis in D-98s cells. J Cell Biol 73: 672–684. doi: 10.1083/jcb.73.3.672 873994

18. Kechad A, Jananji S, Ruella Y, Hickson GR (2012) Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr Biol 22: 197–203. doi: 10.1016/j.cub.2011.11.062 22226749

19. Bassi ZI, Audusseau M, Riparbelli MG, Callaini G, D’Avino PP (2013) Citron kinase controls a molecular network required for midbody formation in cytokinesis. Proc Natl Acad Sci U S A 110: 9782–9787. doi: 10.1073/pnas.1301328110 23716662

20. Green RA, Mayers JR, Wang S, Lewellyn L, Desai A, et al. (2013) The midbody ring scaffolds the abscission machinery in the absence of midbody microtubules. J Cell Biol 203: 505–520. doi: 10.1083/jcb.201306036 24217623

21. 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

22. 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

23. Elia N, Fabrikant G, Kozlov MM, Lippincott-Schwartz J (2012) Computational model of cytokinetic abscission driven by ESCRT-III polymerization and remodeling. Biophys J 102: 2309–2320. doi: 10.1016/j.bpj.2012.04.007 22677384

24. Yang D, Rismanchi N, Renvoise B, Lippincott-Schwartz J, Blackstone C, et al. (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15: 1278–1286. doi: 10.1038/nsmb.1512 18997780

25. Greenbaum MP, Iwamori T, Buchold GM, Matzuk MM (2011) Germ cell intercellular bridges. Cold Spring Harb Perspect Biol 3: a005850. doi: 10.1101/cshperspect.a005850 21669984

26. Haglund K, Nezis IP, Stenmark H (2011) Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development. Commun Integr Biol 4: 1–9. doi: 10.4161/cib.4.1.13550 21509167

27. Robinson DN, Cooley L (1996) Stable intercellular bridges in development: the cytoskeleton lining the tunnel. Trends Cell Biol 6: 474–479. doi: 10.1016/0962-8924(96)84945-2 15157506

28. Lacroix B, Maddox AS (2012) Cytokinesis, ploidy and aneuploidy. J Pathol 226: 338–351. doi: 10.1002/path.3013 21984283

29. 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

30. 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

31. de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125: 2781–2789. 9655801

32. Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9: 257–262. doi: 10.1016/S0962-8924(99)01594-9 10370240

33. Spradling A, Fuller MT, Braun RE, Yoshida S (2011) Germline stem cells. Cold Spring Harb Perspect Biol 3: a002642. doi: 10.1101/cshperspect.a002642 21791699

34. Horne-Badovinac S, Bilder D (2005) Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 232: 559–574. doi: 10.1002/dvdy.20286 15704134

35. Huynh JR, St Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14: R438–449. doi: 10.1016/j.cub.2004.05.040 15182695

36. 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

37. Sheng XR, Matunis E (2011) Live imaging of the Drosophila spermatogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development 138: 3367–3376. doi: 10.1242/dev.065797 21752931

38. Haglund K, Nezis IP, Lemus D, Grabbe C, Wesche J, et al. (2010) Cindr interacts with anillin to control cytokinesis in Drosophila melanogaster. Curr Biol 20: 944–950. doi: 10.1016/j.cub.2010.03.068 20451383

39. Mathe E, Inoue YH, Palframan W, Brown G, Glover DM (2003) Orbit/Mast, the CLASP orthologue of Drosophila, is required for asymmetric stem cell and cystocyte divisions and development of the polarised microtubule network that interconnects oocyte and nurse cells during oogenesis. Development 130: 901–915. doi: 10.1242/dev.00315 12538517

40. Brawley C, Matunis E (2004) Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304: 1331–1334. doi: 10.1126/science.1097676 15143218

41. Eikenes AH, Brech A, Stenmark H, Haglund K (2013) Spatiotemporal control of Cindr at ring canals during incomplete cytokinesis in the Drosophila male germline. Dev Biol 377: 9–20. doi: 10.1016/j.ydbio.2013.02.021 23499247

42. Miyauchi C, Kitazawa D, Ando I, Hayashi D, Inoue YH (2013) Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males. PLoS One 8: e58220. doi: 10.1371/journal.pone.0058220 23520495

43. Yadlapalli S, Yamashita YM (2013) Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 498: 251–254. doi: 10.1038/nature12106 23644460

44. Hudson AM, Cooley L (2014) Methods for studying oogenesis. Methods 68: 207–217. doi: 10.1016/j.ymeth.2014.01.005 24440745

45. 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

46. Yan D, Neumuller RA, Buckner M, Ayers K, Li H, et al. (2014) A regulatory network of Drosophila germline stem cell self-renewal. Dev Cell 28: 459–473. doi: 10.1016/j.devcel.2014.01.020 24576427

47. Lilly MA, de Cuevas M, Spradling AC (2000) Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Dev Biol 218: 53–63. doi: 10.1006/dbio.1999.9570 10644410

48. 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

49. 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

50. Deng W, Lin H (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol 189: 79–94. doi: 10.1006/dbio.1997.8669 9281339

51. Hsu HJ, LaFever L, Drummond-Barbosa D (2008) Diet controls normal and tumorous germline stem cells via insulin-dependent and-independent mechanisms in Drosophila. Dev Biol 313: 700–712. doi: 10.1016/j.ydbio.2007.11.006 18068153

52. McCullough J, Colf LA, Sundquist WI (2013) Membrane fission reactions of the mammalian ESCRT pathway. Annu Rev Biochem 82: 663–692. doi: 10.1146/annurev-biochem-072909-101058 23527693

53. Guizetti J, Gerlich DW (2012) ESCRT-III polymers in membrane neck constriction. Trends Cell Biol 22: 133–140. doi: 10.1016/j.tcb.2011.11.007 22240455

54. McCullough J, Fisher RD, Whitby FG, Sundquist WI, Hill CP (2008) ALIX-CHMP4 interactions in the human ESCRT pathway. Proc Natl Acad Sci U S A 105: 7687–7691. doi: 10.1073/pnas.0801567105 18511562

55. Matias NR, Mathieu J, Huynh JR (2015) Abscission is regulated by the ESCRT-III protein Shrub in Drosophila germline stem cells. PLoS Genet. 11: e1004653.

56. Lindas AC, Karlsson EA, Lindgren MT, Ettema TJ, Bernander R (2008) A unique cell division machinery in the Archaea. Proc Natl Acad Sci U S A 105: 18942–18946. doi: 10.1073/pnas.0809467105 18987308

57. Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in archaea. Science 322: 1710–1713. doi: 10.1126/science.1165322 19008417

58. Lindas AC, Bernander R (2013) The cell cycle of archaea. Nat Rev Microbiol 11: 627–638. doi: 10.1038/nrmicro3077 23893102

59. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, et al. (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133: 4679–4689. doi: 10.1242/dev.02654 17090720

60. McMurray MA, Stefan CJ, Wemmer M, Odorizzi G, Emr SD, et al. (2011) Genetic interactions with mutations affecting septin assembly reveal ESCRT functions in budding yeast cytokinesis. Biol Chem 392: 699–712. doi: 10.1515/BC.2011.091 21824003

61. Renshaw MJ, Liu J, Lavoie BD, Wilde A (2014) Anillin-dependent organization of septin filaments promotes intercellular bridge elongation and Chmp4B targeting to the abscission site. Open Biol 4: 130190. doi: 10.1098/rsob.130190 24451548

62. Mondal G, Rowley M, Guidugli L, Wu J, Pankratz VS, et al. (2012) BRCA2 localization to the midbody by filamin A regulates cep55 signaling and completion of cytokinesis. Dev Cell 23: 137–152. doi: 10.1016/j.devcel.2012.05.008 22771033

63. Sagona AP, Nezis IP, Pedersen NM, Liestol K, Poulton J, et al. (2010) PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat Cell Biol 12: 362–371. doi: 10.1038/ncb2036 20208530

64. Neto H, Kaupisch A, Collins LL, Gould GW (2013) Syntaxin 16 is a master recruitment factor for cytokinesis. Mol Biol Cell 24: 3663–3674. doi: 10.1091/mbc.E13-06-0302 24109596

65. Pires R, Hartlieb B, Signor L, Schoehn G, Lata S, et al. (2009) A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments. Structure 17: 843–856. doi: 10.1016/j.str.2009.04.007 19523902

66. Kim J, Sitaraman S, Hierro A, Beach BM, Odorizzi G, et al. (2005) Structural basis for endosomal targeting by the Bro1 domain. Dev Cell 8: 937–947. doi: 10.1016/j.devcel.2005.04.001 15935782

67. Wemmer M, Azmi I, West M, Davies B, Katzmann D, et al. (2011) Bro1 binding to Snf7 regulates ESCRT-III membrane scission activity in yeast. J Cell Biol 192: 295–306. doi: 10.1083/jcb.201007018 21263029

68. Bissig C, Gruenberg J (2013) ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol 24: 19–25. doi: 10.1016/j.tcb.2013.10.009 24287454

69. Dobro MJ, Samson RY, Yu Z, McCullough J, Ding HJ, et al. (2013) Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggests that spiraling filaments are involved in membrane scission. Mol Biol Cell 24: 2319–2327. doi: 10.1091/mbc.E12-11-0785 23761076

70. 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

71. 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

72. 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

73. Ohlstein B, McKearin D (1997) Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124: 3651–3662. 9342057

74. Sweeney NT, Brenman JE, Jan YN, Gao FB (2006) The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr Biol 16: 1006–1011. doi: 10.1016/j.cub.2006.03.067 16713958

75. Luo L, Chai PC, Cai Y (2013) Immunostaining of germline stem cells and the niche in Drosophila ovaries. Methods Mol Biol 1035: 1–7. doi: 10.1007/978-1-62703-508-8_1 23959977

76. D’Avino PP, Archambault V, Przewloka MR, Zhang W, Laue ED, et al. (2009) Isolation of protein complexes involved in mitosis and cytokinesis from Drosophila cultured cells. Methods Mol Biol 545: 99–112. doi: 10.1007/978-1-60327-993-2_6 19475384

77. Venken KJ, Carlson JW, Schulze KL, Pan H, He Y, et al. (2009) Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods 6: 431–434. doi: 10.1038/nmeth.1331 19465919

78. Rothwell WF, Sullivan W (2007) Fixation of Drosophila embryos. CSH Protoc 2007: pdb prot4827

79. Woodruff RI, Tilney LG (1998) Intercellular bridges between epithelial cells in the Drosophila ovarian follicle: a possible aid to localized signaling. Dev Biol 200: 82–91. doi: 10.1006/dbio.1998.8948 9698458

80. Airoldi SJ, McLean PF, Shimada Y, Cooley L (2011) Intercellular protein movement in syncytial Drosophila follicle cells. Journal of Cell Science 124: 4077–4086. doi: 10.1242/jcs.090456 22135360

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#