OSD1 Promotes Meiotic Progression via APC/C Inhibition and Forms a Regulatory Network with TDM and CYCA1;2/TAM
Cell cycle control is modified at meiosis compared to mitosis, because two divisions follow a single DNA replication event. Cyclin-dependent kinases (CDKs) promote progression through both meiosis and mitosis, and a central regulator of their activity is the APC/C (Anaphase Promoting Complex/Cyclosome) that is especially required for exit from mitosis. We have shown previously that OSD1 is involved in entry into both meiosis I and meiosis II in Arabidopsis thaliana; however, the molecular mechanism by which OSD1 controls these transitions has remained unclear. Here we show that OSD1 promotes meiotic progression through APC/C inhibition. Next, we explored the functional relationships between OSD1 and the genes known to control meiotic cell cycle transitions in Arabidopsis. Like osd1, cyca1;2/tam mutation leads to a premature exit from meiosis after the first division, while tdm mutants perform an aberrant third meiotic division after normal meiosis I and II. Remarkably, while tdm is epistatic to tam, osd1 is epistatic to tdm. We further show that the expression of a non-destructible CYCA1;2/TAM provokes, like tdm, the entry into a third meiotic division. Finally, we show that CYCA1;2/TAM forms an active complex with CDKA;1 that can phosphorylate OSD1 in vitro. We thus propose that a functional network composed of OSD1, CYCA1;2/TAM, and TDM controls three key steps of meiotic progression, in which OSD1 is a meiotic APC/C inhibitor.
Vyšlo v časopise:
OSD1 Promotes Meiotic Progression via APC/C Inhibition and Forms a Regulatory Network with TDM and CYCA1;2/TAM. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002865
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002865
Souhrn
Cell cycle control is modified at meiosis compared to mitosis, because two divisions follow a single DNA replication event. Cyclin-dependent kinases (CDKs) promote progression through both meiosis and mitosis, and a central regulator of their activity is the APC/C (Anaphase Promoting Complex/Cyclosome) that is especially required for exit from mitosis. We have shown previously that OSD1 is involved in entry into both meiosis I and meiosis II in Arabidopsis thaliana; however, the molecular mechanism by which OSD1 controls these transitions has remained unclear. Here we show that OSD1 promotes meiotic progression through APC/C inhibition. Next, we explored the functional relationships between OSD1 and the genes known to control meiotic cell cycle transitions in Arabidopsis. Like osd1, cyca1;2/tam mutation leads to a premature exit from meiosis after the first division, while tdm mutants perform an aberrant third meiotic division after normal meiosis I and II. Remarkably, while tdm is epistatic to tam, osd1 is epistatic to tdm. We further show that the expression of a non-destructible CYCA1;2/TAM provokes, like tdm, the entry into a third meiotic division. Finally, we show that CYCA1;2/TAM forms an active complex with CDKA;1 that can phosphorylate OSD1 in vitro. We thus propose that a functional network composed of OSD1, CYCA1;2/TAM, and TDM controls three key steps of meiotic progression, in which OSD1 is a meiotic APC/C inhibitor.
Zdroje
1. de GramontACohen-FixO 2005 The many phases of anaphase. Trends in biochemical sciences 30 559 568 doi:10.1016/j.tibs.2005.08.008
2. Pérez-HidalgoLMorenoSMartín-CastellanosC 2008 Modified cell cycle regulation in meiosis. EgelRLankenauD-H Recombination and Meiosis Springer Berlin/Heidelberg, Vol. 2 307 353 doi:10.1007/7050_2007_029
3. Pesin JaOrr-WeaverTL 2008 Regulation of APC/C activators in mitosis and meiosis. Annual review of cell and developmental biology 24 475 499 doi:10.1146/annurev.cellbio.041408.115949
4. FülöpKTarayreSKelemenZHorváthGKeveiZ 2005 Arabidopsis anaphase-promoting complexes: multiple activators and wide range of substrates might keep APC perpetually busy. Cell cycle 4 1084 1092 doi:10.1111/j.1872-034X.2011.00940.x
5. KeveiZBalobanMDa InesOTiriczHKrollA 2011 Conserved CDC20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana. PloS ONE 6 e20618 doi:10.1371/journal.pone.0020618
6. FurunoNNishizawaMOkazakiKTanakaHIwashitaJ 1994 Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes. The EMBO journal 13 2399 2410
7. OheMInoueDKanemoriYSagataN 2007 Erp1/Emi2 is essential for the meiosis I to meiosis II transition in Xenopus oocytes. Developmental biology 303 157 164 doi:10.1016/j.ydbio.2006.10.044
8. MadgwickSHansenDVLevasseurMJacksonPKJonesKT 2006 Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. The Journal of cell biology 174 791 801 doi:10.1083/jcb.200604140
9. KimataYKitamuraKFennerNYamanoH 2011 Mes1 controls the meiosis I to meiosis II transition by distinctly regulating APC/C co-activators Fzr1/Mfr1 and Slp1 in fission yeast. Molecular biology of the cell doi:10.1091/mbc.E10-09-0774
10. KimataYTrickeyMIzawaDGannonJYamamotoM 2008 A mutual inhibition between APC/C and its substrate Mes1 required for meiotic progression in fission yeast. Developmental cell 14 446 454 doi:10.1016/j.devcel.2007.12.010
11. IzawaDGotoMYamashitaAYamanoHYamamotoM 2005 Fission yeast Mes1p ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p. Nature 434 529 533 doi:10.1038/nature03406
12. DissmeyerNNowackMKPuschSStalsHInzéD 2007 T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. The Plant cell 19 972 985 doi:10.1105/tpc.107.050401
13. BulankovaPRiehs-KearnanNNowackMKSchnittgerARihaK 2010 Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. The Plant cell 22 3791 3803 doi:10.1105/tpc.110.078378
14. HarashimaHSchnittgerA n.d. Robust reconstitution of active cell-cycle control complexes from co-expressed proteins in bacteria. Plant Methods in press
15. d' ErfurthICromerLJolivetSGirardCHorlowC 2010 The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6 e1000989 doi:10.1371/journal.pgen.1000989
16. d' ErfurthIJolivetSFrogerNCatriceONovatchkovaM 2009 Turning meiosis into mitosis. PLoS Biol 7 e1000124 doi:10.1371/journal.pbio.1000124
17. WangYJhaAKChenRDoonanJHYangM 2010 Polyploidy-associated genomic instability in Arabidopsis thaliana. Genesis 48 254 263 doi:10.1002/dvg.20610
18. WangYMagnardJLMcCormickSYangM 2004 Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant physiology 136 4127 doi:10.1104/pp.104.051201.1
19. IwataEIkedaSMatsunagaSKurataMYoshiokaY 2011 GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis. The Plant cell 23 4382 4393 doi:10.1105/tpc.111.092049
20. RossKJFranszPArmstrongSJVizirIMulliganB 1997 Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Research 5 551 559
21. GloverJGrelonMCraigSChaudhuryADennisE 1998 Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. The Plant journal: for cell and molecular biology 15 345 356
22. RiehsNAkimchevaSPuizinaJBulankovaPIdol Ra 2008 Arabidopsis SMG7 protein is required for exit from meiosis. Journal of cell science 121 2208 2216 doi:10.1242/jcs.027862
23. HayesMJKimataYWattamSLLindonCMaoG 2006 Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nature cell biology 8 607 614 doi:10.1038/ncb1410
24. OheMKawamuraYUenoHInoueDKanemoriY 2010 Emi2 inhibition of the anaphase-promoting complex/cyclosome absolutely requires Emi2 binding via the C-terminal RL tail. Molecular biology of the cell 21 905 913 doi:10.1091/mbc.E09-11-0974
25. Van LeeneJHollunderJEeckhoutDPersiauGVan De SlijkeE 2010 Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Molecular systems biology 6 397 doi:10.1038/msb.2010.53
26. WangGKongHSunYZhangXZhangW 2004 Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant physiology 135 1084 1099 doi:10.1104/pp.104.040436
27. HaseYTrungKHMatsunagaTTanakaA 2006 A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. The Plant journal: for cell and molecular biology 46 317 326 doi:10.1111/j.1365-313X.2006.02696.x
28. HeymanJVan den DaeleHDe WitKBoudolfVBerckmansB 2011 Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 Maintains Cell Division Activity by Temporal Inhibition of the Anaphase-Promoting Complex/Cyclosome. The Plant cell 1 doi:10.1105/tpc.111.091793
29. BiegertAMayerCRemmertMSödingJLupasAN 2006 The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic acids research 34 W335 9 doi:10.1093/nar/gkl217
30. SödingJBiegertALupasAN 2005 The HHpred interactive server for protein homology detection and structure prediction. Nucleic acids research 33 W244 8 doi:10.1093/nar/gki408
31. AzumiYLiuDZhaoDLiWWangG 2002 Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. The EMBO journal 21 3081 3095 doi:10.1093/emboj/cdf285
32. De MuytAPereiraLVezonDChelyshevaLGendrotG 2009 A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5 e1000654 doi:10.1371/journal.pgen.1000654
33. TangWWuJQGuoYHansenDVPerryJA 2008 Cdc2 and Mos regulate Emi2 stability to promote the meiosis I-meiosis II transition. Molecular biology of the cell 19 3536 3543 doi:10.1091/mbc.E08-04-0417
34. IsodaMSakoKSuzukiKNishinoKNakajoN 2011 Dynamic regulation of Emi2 by Emi2-bound Cdk1/Plk1/CK1 and PP2A-B56 in meiotic arrest of Xenopus eggs. Developmental cell 21 506 519 doi:10.1016/j.devcel.2011.06.029
35. VignardJSiwiecTChelyshevaLVrielynckNGonordF 2007 The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3 e176 doi:10.1371/journal.pgen.0030176
36. EstelleMASomervilleC 1987 Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. MGG Molecular & General Genetics 206 200 206 doi:10.1007/BF00333575
37. NotredameCHigginsDGHeringaJ 2000 T-Coffee: A novel method for fast and accurate multiple sequence alignment. Journal of molecular biology 302 205 217 doi:10.1006/jmbi.2000.4042
38. Van LeeneJStalsHEeckhoutDPersiauGVan De SlijkeE 2007 A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Molecular & cellular proteomics: MCP 6 1226 1238 doi:10.1074/mcp.M700078-MCP200
39. HachedKXieSZBuffinECladièreDRachezC 2011 Mps1 at kinetochores is essential for female mouse meiosis I. Development (Cambridge, England) 138 2261 2271 doi:10.1242/dev.061317
40. BussoDDelagoutte-BussoBMorasD 2005 Construction of a set Gateway-based destination vectors for high-throughput cloning and expression screening in Escherichia coli. Analytical biochemistry 343 313 321 doi:10.1016/j.ab.2005.05.015
41. RossKJFranszPJonesGH 1996 A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Research 4 507 516
42. MotamayorJCVezonDBajonCSauvanetAGrandjeanO 2000 Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sexual Plant Reproduction 12 209 218
43. AlexanderM 1969 Differential staining of aborted and nonaborted pollen. Biotechnic & Histochemistry 44 117 122
44. MercierRVezonDBullierEMotamayorJCSellierA 2001 SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes & development 15 1859 1871 doi:10.1101/gad.203201
45. NakagawaTKuroseTHinoTTanakaKKawamukaiM 2007 Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of bioscience and bioengineering 104 34 41 doi:10.1263/jbb.104.34
46. CloughSJBentAF 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant journal: for cell and molecular biology 16 735 743
47. HorvathARiezmanH 1994 Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10 1305 1310
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 7
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Guidelines for Genome-Wide Association Studies
- The Role of Rice HEI10 in the Formation of Meiotic Crossovers
- Identification of Chromatin-Associated Regulators of MSL Complex Targeting in Dosage Compensation
- GWAS Identifies Novel Susceptibility Loci on 6p21.32 and 21q21.3 for Hepatocellular Carcinoma in Chronic Hepatitis B Virus Carriers