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The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition


Autoři: Daniela Torres-Campana aff001;  Shuhei Kimura aff002;  Guillermo A. Orsi aff001;  Béatrice Horard aff001;  Gérard Benoit aff001;  Benjamin Loppin aff001
Působiště autorů: Laboratoire de Biologie et de Modélisation de la Cellule, CNRS UMR5239, Ecole Normale Supérieure de Lyon, University of Lyon, France aff001;  Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, CNRS, UMR 5558, Villeurbanne F-69622, France aff002
Vyšlo v časopise: The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. PLoS Genet 16(3): e1008543. doi:10.1371/journal.pgen.1008543
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008543

Souhrn

Following fertilization of a mature oocyte, the formation of a diploid zygote involves a series of coordinated cellular events that ends with the first embryonic mitosis. In animals, this complex developmental transition is almost entirely controlled by maternal gene products. How such a crucial transcriptional program is established during oogenesis remains poorly understood. Here, we have performed an shRNA-based genetic screen in Drosophila to identify genes required to form a diploid zygote. We found that the Lid/KDM5 histone demethylase and its partner, the Sin3A-HDAC1 deacetylase complex, are necessary for sperm nuclear decompaction and karyogamy. Surprisingly, transcriptomic analyses revealed that these histone modifiers are required for the massive transcriptional activation of deadhead (dhd), which encodes a maternal thioredoxin involved in sperm chromatin remodeling. Unexpectedly, while lid knock-down tends to slightly favor the accumulation of its target, H3K4me3, on the genome, this mark was lost at the dhd locus. We propose that Lid/KDM5 and Sin3A cooperate to establish a local chromatin environment facilitating the unusually high expression of dhd, a key effector of the oocyte-to-zygote transition.

Klíčová slova:

Drosophila melanogaster – Embryos – Fertilization – Gene expression – Histones – Chromatin – Ovaries – Sperm


Zdroje

1. Loppin B, Dubruille R, Horard B (2015) The intimate genetics of Drosophila fertilization. Open Biol 5: 150076. doi: 10.1098/rsob.150076 26246493

2. Hamm DC, Harrison MM (2018) Regulatory principles governing the maternal-to-zygotic transition: insights from Drosophila melanogaster. Open Biol 8: 180183. doi: 10.1098/rsob.180183 30977698

3. Spradling AC (1993) Developmental genetics of oogenesis. The Development of Drosophila melanogaster—Cold Spring Harbor Laboratory Press. 1–69.

4. Eirin-López JM, Ausió J (2009) Origin and evolution of chromosomal sperm proteins. Bioessays 31: 1062–1070. doi: 10.1002/bies.200900050 19708021

5. Rathke C, Baarends WM, Awe S, Renkawitz-Pohl R (2014) Chromatin dynamics during spermiogenesis. Biochim Biophys Acta. 1839: 155–168. doi: 10.1016/j.bbagrm.2013.08.004 24091090

6. Tirmarche S, Kimura S, Dubruille R, Horard B, Loppin B (2016) Unlocking sperm chromatin at fertilization requires a dedicated egg thioredoxin in Drosophila. Nature Commun 7: 13539. https://doi:10.1038/ncomms13539

7. Petrova B, Liu K, Tian C, Kitaoka M, Freinkman E, Yang J, et al. (2018) Dynamic redox balance directs the oocyte-to-embryo transition via developmentally controlled reactive cysteine changes. Proc Natl Acad Sci USA 115: E7978–E7986. doi: 10.1073/pnas.1807918115 30082411

8. Horard B, Sapey-Triomphe L, Bonnefoy E, Loppin B (2018) ASF1 is required to load histoneson the HIRA complex in preparation of paternal chromatin assembly at fertilization. Epigenetics Chromatin 11: 19. doi: 10.1186/s13072-018-0189-x 29751847

9. Ni J-Q, Zhou R, Czech B, Liu L-P, Holderbaum L, Yang-Zhou D, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Meth 8: 405–407. https://doi:10.1038/nmeth.1592

10. Delabaere L, Orsi GA, Sapey-Triomphe L, Horard B, Couble P, Loppin B (2014) The Spartan Ortholog Maternal Haploid Is Required for Paternal Chromosome Integrity in the Drosophila Zygote. Curr Biol 24: 2281–2287. doi: 10.1016/j.cub.2014.08.010 25242033

11. Gildea JJ, Lopez R, Shearn A (2000) A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics 156: 645–663. 11014813

12. Secombe J, Li L, Carlos L, Eisenman RN (2007) The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes & Dev 21: 537–551. https://doi:10.1101/gad.1523007

13. Lloret-Llinares M, Carr CM, Vaquero A, de Olano N, Azorin F (2008) Characterization of Drosophila melanogaster JmjC+N histone demethylases. Nucleic Acids Res. 36: 2852–2863. doi: 10.1093/nar/gkn098 18375980

14. Lloret-Llinares M, Perez-Lluch S, Rossell D, Moran T, Ponsa-Cobas J, Auer H, et al. (2012) dKDM5/LID regulates H3K4me3 dynamics at the transcription-start site (TSS) of actively transcribed developmental genes. Nucleic Acids Res. 40: 9493–9505. doi: 10.1093/nar/gks773 22904080

15. Grzenda A, Lomberk G, Zhang J-S, Urrutia R (2009) Sin3: Master scaffold and transcriptional corepressor. Biochim Biophys Acta 1789: 443–450. doi: 10.1016/j.bbagrm.2009.05.007 19505602

16. Spain MM, Caruso JA, Swaminathan A, Pile LA (2010) Drosophila SIN3 Isoforms Interact with Distinct Proteins and Have Unique Biological Functions. J Biol Chem 285: 27457–27467. doi: 10.1074/jbc.M110.130245 20566628

17. Gajan A, Barnes VL, Liu M, Saha N, Pile LA (2016) The histone demethylase dKDM5/LID interacts with the SIN3 histone deacetylase complex and shares functional similarities with SIN3. Epigenetics Chromatin 9:4 doi: 10.1186/s13072-016-0053-9 26848313

18. Liu M, Pile LA (2017) The Transcriptional Corepressor SIN3 Directly Regulates Genes Involved in Methionine Catabolism and Affects Histone Methylation, Linking Epigenetics and Metabolism. J Biol Chem 292: 1970–1976. doi: 10.1074/jbc.M116.749754 28028175

19. Barnes VL, Bhat A, Unnikrishnan A, Heydari AR, Arking R, Pile LA (2014) SIN3 is critical for stress resistance and modulates adult lifespan. Aging 6: 645–660. doi: 10.18632/aging.100684 25133314

20. Moshkin YM, Kan TW, Goodfellow H, Bezstarosti K, Maeda RK, Pilyugin M, et al. (2009) Histone Chaperones ASF1 and NAP1 Differentially Modulate Removal of Active Histone Marks by LID-RPD3 Complexes during NOTCH Silencing. Mol Cell 35: 782–793. doi: 10.1016/j.molcel.2009.07.020 19782028

21. Lee N, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2009) The H3K4 Demethylase Lid Associates with and Inhibits Histone Deacetylase Rpd3. Mol Cell Biol 29: 1401–1410. doi: 10.1128/MCB.01643-08 19114561

22. Kronja I, Yuan B, Eichhorn SW, Dzeyk K, Krijgsveld J, Bartel DP, et al. (2014) Widespread Changesin the Posttranscriptional Landscapeat the Drosophila Oocyte-to-Embryo Transition. Cell Reports 7: 1495–1508. doi: 10.1016/j.celrep.2014.05.002 24882012

23. Navarro-Costa P, McCarthy A, Prudêncio P, Greer C, Guilgur LG, Becker JORD, et al. (2016) Early programming of the oocyte epigenome temporally controls late prophase I transcription and chromatin remodelling. Nature Commun 7: 1–15. https://doi:10.1038/ncomms12331

24. Manier MK, Belote JM, Berben KS, Novikov D, Stuart WT, Pitnick S (2010) Resolving Mechanisms of Competitive Fertilization Success in Drosophila melanogaster. Science 328: 354–357. doi: 10.1126/science.1187096 20299550

25. Zhaunova L, Ohkura H, Breuer M (2016) Kdm5/Lid Regulates Chromosome Architecture in Meiotic Prophase I Independently of Its Histone Demethylase Activity. PLoS Genet. 12: e1006241. doi: 10.1371/journal.pgen.1006241 27494704

26. Drelon C, Belalcazar HM, Secombe J. The Histone Demethylase KDM5 Is Essential for Larval Growth in Drosophila (2018) Genetics 209: 773–787. doi: 10.1534/genetics.118.301004 29764901

27. Liu X, Secombe J (2015) The Histone Demethylase KDM5 Activates Gene Expression by Recognizing Chromatin Context through Its PHD Reader Motif. Cell Reports 13: 2219–2231. doi: 10.1016/j.celrep.2015.11.007 26673323

28. Emelyanov AV, Fyodorov DV (2016) Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin. Genes & Dev 30: 2651–2656. https://doi:10.1101/gad.290916.116

29. Sandler JE, Stathopoulos A (2016) Quantitative Single-Embryo Profile of Drosophila Genome Activation and the Dorsal-Ventral Patterning Network. Genetics 202: 1575–1584. doi: 10.1534/genetics.116.186783 26896327

30. Zamurrad S, Hatch HAM, Drelon C, Belalcazar HM, Secombe J (2018) A Drosophila Model of Intellectual Disability Caused by Mutations in the Histone Demethylase KDM5. Cell Reports 22: 2359–2369. doi: 10.1016/j.celrep.2018.02.018 29490272

31. Li L, Greer C, Eisenman RN, Secombe J (2010) Essential functions of the histone demethylase lid. PLoS Genet. 6: e1001221. doi: 10.1371/journal.pgen.1001221 21124823

32. Lussi YC, Mariani L, Friis C, Peltonen J, Myers TR, Krag C, et al. (2016) Impaired removal of H3K4 methylation affects cell fate determination and gene transcription. Development 143: 3751–3762. doi: 10.1242/dev.139139 27578789

33. Kidder BL, Hu G, Zhao K (2014) KDM5B focuses H3K4 methylation near promoters and enhancers during embryonic stem cell self-renewal and differentiation. Genome Biol 15: R32. doi: 10.1186/gb-2014-15-2-r32 24495580

34. Outchkourov NS, Muiño JM, Kaufmann K, van IJcken WFJ, Koerkamp MJG, van Leenen D, et al. (2013) Balancing of Histone H3K4 Methylation States by the Kdm5c/SMCX Histone Demethylase Modulates Promoter and Enhancer Function. Cell Reports 3: 1071–1079. doi: 10.1016/j.celrep.2013.02.030 23545502

35. Freeman M, Nüsslein-Volhard C, Glover DM (1986) The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell 46: 457–468. doi: 10.1016/0092-8674(86)90666-5 3089628

36. Herz HM, Mohan M, Garruss AS, Liang K, Takahashi YH, Mickey K, et al. (2012) Enhancer-associated H3K4 monomethylation by Trithorax-related, the Drosophila homolog of mammalian Mll3/Mll4. Genes & Dev 26: 2604–2620. https://doi:10.1101/gad.201327.112

37. Prudêncio P, Guilgur LG, Sobral J, Becker JD, Martinho RG, Navarro-Costa P (2018) The Trithorax group protein dMLL3/4 instructs the assembly of the zygotic genome at fertilization. EMBO Rep 19: e45728. doi: 10.15252/embr.201845728 30037897

38. 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. doi: 10.1016/j.cub.2006.11.051 17222555

39. Salz HK, Flickinger TW, Mittendorf E, Pellicena-Palle A, Petschek JP, Brown Albretch E (1994) The Drosophila Maternal Effect Locus deadhead Encodes a Thioredoxin Homolog Required for Female Meiosis and Early Embryonic Development. Genetics 136: 1075–1086. 7516301

40. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262 11846609

41. Grentzinger T, Armenise C, Brun C, Mugat B, Serrano V, Pelisson A, et al. (2012) piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res 22: 1877–1888. doi: 10.1101/gr.136614.111 22555593


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