Active transcription and Orc1 drive chromatin association of the AAA+ ATPase Pch2 during meiotic G2/prophase

English version

Autoři: Richard Cardoso da Silva ^aff001; María Ascensión Villar-Fernández ^aff001; Gerben Vader ^aff001
Působiště autorů: Department of Mechanistic Cell Biology, Max Planck Institute of Molecular Physiology, Dortmund, Germany ^aff001; International Max Planck Research School (IMPRS) in Chemical and Molecular Biology, Max Planck Institute of Molecular Physiology, Dortmund, Germany ^aff002
Vyšlo v časopise: Active transcription and Orc1 drive chromatin association of the AAA+ ATPase Pch2 during meiotic G2/prophase. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008905
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008905

Souhrn

Pch2 is an AAA+ protein that controls DNA break formation, recombination and checkpoint signaling during meiotic G2/prophase. Chromosomal association of Pch2 is linked to these processes, and several factors influence the association of Pch2 to euchromatin and the specialized chromatin of the ribosomal (r)DNA array of budding yeast. Here, we describe a comprehensive mapping of Pch2 localization across the budding yeast genome during meiotic G2/prophase. Within non-rDNA chromatin, Pch2 associates with a subset of actively RNA Polymerase II (RNAPII)-dependent transcribed genes. Chromatin immunoprecipitation (ChIP)- and microscopy-based analysis reveals that active transcription is required for chromosomal recruitment of Pch2. Similar to what was previously established for association of Pch2 with rDNA chromatin, we find that Orc1, a component of the Origin Recognition Complex (ORC), is required for the association of Pch2 to these euchromatic, transcribed regions, revealing a broad connection between chromosomal association of Pch2 and Orc1/ORC function. Ectopic mitotic expression is insufficient to drive recruitment of Pch2, despite the presence of active transcription and Orc1/ORC in mitotic cells. This suggests meiosis-specific ‘licensing’ of Pch2 recruitment to sites of transcription, and accordingly, we find that the synaptonemal complex (SC) component Zip1 is required for the recruitment of Pch2 to transcription-associated binding regions. Interestingly, Pch2 binding patterns are distinct from meiotic axis enrichment sites (as defined by Red1, Hop1, and Rec8). Inactivating RNAPII-dependent transcription/Orc1 does not lead to effects on the chromosomal abundance of Hop1, a known chromosomal client of Pch2, suggesting a complex relationship between SC formation, Pch2 recruitment and Hop1 chromosomal association. We thus report characteristics and dependencies for Pch2 recruitment to meiotic chromosomes, and reveal an unexpected link between Pch2, SC formation, chromatin and active transcription.

Klíčová slova:

Binding analysis – DNA transcription – Histones – Chromatin – Chromosome structure and function – Immunofluorescence – Meiosis – Synapsis

Zdroje

1. Petronczki M, Siomos MF, Nasmyth K. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell. 2003;112(4):423–40. doi: 10.1016/s0092-8674(03)00083-7 12600308

2. Lam I, Keeney S. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol. 2015;7(1):a016634.

3. Moens PB, Pearlman RE. Chromatin organization at meiosis. BioEssays. 1988;9(5):151–3. doi: 10.1002/bies.950090503 3071365

4. Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. doi: 10.1146/annurev.genet.33.1.603 10690419

5. Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2 2107981

6. Smith AV, Roeder GS. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol. 1997;136(5):957–67. doi: 10.1083/jcb.136.5.957 9060462

7. West AM, Rosenberg SC, Ur SN, Lehmer MK, Ye Q, Hagemann G, et al. A conserved filamentous assembly underlies the structure of the meiotic chromosome axis. eLife. 2019;8.

8. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell. 2011;146(3):372–83. doi: 10.1016/j.cell.2011.07.003 21816273

9. Sun X, Huang L, Markowitz TE, Blitzblau HG, Chen D, Klein F, et al. Transcription dynamically patterns the meiotic chromosome-axis interface. eLife. 2015;4.

10. Page SL, Hawley RS. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–58. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851

11. Agarwal S, Roeder GS. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell. 2000;102(2):245–55. doi: 10.1016/s0092-8674(00)00029-5 10943844

12. Henderson KA, Keeney S. Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci U S A. 2004;101(13):4519–24. doi: 10.1073/pnas.0400843101 15070750

13. Sym M, Engebrecht JA, Roeder GS. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993;72(3):365–78. doi: 10.1016/0092-8674(93)90114-6 7916652

14. Tung KS, Roeder GS. Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics. 1998;149(2):817–32. 9611194

15. Subramanian VV, MacQueen AJ, Vader G, Shinohara M, Sanchez A, Borde V, et al. Chromosome Synapsis Alleviates Mek1-Dependent Suppression of Meiotic DNA Repair. PLoS Biol. 2016;14(2):e1002369. doi: 10.1371/journal.pbio.1002369 26870961

16. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY, et al. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 2013;9(12):e1003978. doi: 10.1371/journal.pgen.1003978 24367271

17. Thacker D, Mohibullah N, Zhu X, Keeney S. Homologue engagement controls meiotic DNA break number and distribution. Nature. 2014;510(7504):241–6. doi: 10.1038/nature13120 24717437

18. San-Segundo PA, Roeder GS. Pch2 links chromatin silencing to meiotic checkpoint control. Cell. 1999;97(3):313–24. doi: 10.1016/s0092-8674(00)80741-2 10319812

19. Roig I, Dowdle JA, Toth A, de Rooij DG, Jasin M, Keeney S. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet. 2010;6(8):e1001062. doi: 10.1371/journal.pgen.1001062 20711356

20. Vader G. Pch2(TRIP13): controlling cell division through regulation of HORMA domains. Chromosoma. 2015;124(3):333–9. doi: 10.1007/s00412-015-0516-y 25895724

21. Mitra N, Roeder GS. A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics. 2007;176(2):773–87. doi: 10.1534/genetics.107.071100 17435220

22. San-Segundo PA, Roeder GS. Role for the silencing protein Dot1 in meiotic checkpoint control. Mol Biol Cell. 2000;11(10):3601–15. doi: 10.1091/mbc.11.10.3601 11029058

23. Ontoso D, Acosta I, van Leeuwen F, Freire R, San-Segundo PA. Dot1-dependent histone H3K79 methylation promotes activation of the Mek1 meiotic checkpoint effector kinase by regulating the Hop1 adaptor. PLoS Genet. 2013;9(1):e1003262. doi: 10.1371/journal.pgen.1003262 23382701

24. Heldrich J, Sun X, Vale-Silva LA, Markowitz TE, Hochwagen A. Topoisomerases modulate the timing of meiotic DNA breakage and chromosome morphogenesis in Saccharomyces cerevisiae. Genetics. 2020; 215 (1):59–73 doi: 10.1534/genetics.120.303060 32152049

25. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 2009;5(10):e1000702. doi: 10.1371/journal.pgen.1000702 19851446

26. Ye Q, Kim DH, Dereli I, Rosenberg SC, Hagemann G, Herzog F, et al. The AAA+ ATPase TRIP13 remodels HORMA domains through N-terminal engagement and unfolding. EMBO J. 2017;36(16):2419–34. doi: 10.15252/embj.201797291 28659378

27. Chen C, Jomaa A, Ortega J, Alani EE. Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A. 2014;111(1):E44–53. doi: 10.1073/pnas.1310755111 24367111

28. Ye Q, Rosenberg SC, Moeller A, Speir JA, Su TY, Corbett KD. TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching. eLife. 2015;4.

29. Yang C, Sofroni K, Wijnker E, Hamamura Y, Carstens L, Harashima H, et al. The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis. EMBO J. 2020;39(3):e101625. doi: 10.15252/embj.2019101625 31556459

30. Vader G, Blitzblau HG, Tame MA, Falk JE, Curtin L, Hochwagen A. Protection of repetitive DNA borders from self-induced meiotic instability. Nature. 2011;477(7362):115–9. doi: 10.1038/nature10331 21822291

31. Bell SP, Kaguni JM. Helicase loading at chromosomal origins of replication. Cold Spring Harb Perspect Biol. 2013;5(6).

32. Wu HY, Burgess SM. Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol. 2006;16(24):2473–9. doi: 10.1016/j.cub.2006.10.069 17174924

33. Ho HC, Burgess SM. Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet. 2011;7(11):e1002351. doi: 10.1371/journal.pgen.1002351 22072981

34. Hanson PI, Whiteheart SW. AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol. 2005;6(7):519–29. doi: 10.1038/nrm1684 16072036

35. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106. doi: 10.1186/gb-2010-11-10-r106 20979621

36. Teytelman L, Thurtle DM, Rine J, van Oudenaarden A. Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc Natl Acad Sci U S A. 2013;110(46):18602–7. doi: 10.1073/pnas.1316064110 24173036

37. Cramer P. Organization and regulation of gene transcription. Nature. 2019;573(7772):45–54. doi: 10.1038/s41586-019-1517-4 31462772

38. Alfieri C, Chang L, Barford D. Mechanism for remodelling of the cell cycle checkpoint protein MAD2 by the ATPase TRIP13. Nature. 2018;559(7713):274–8. doi: 10.1038/s41586-018-0281-1 29973720

39. Herruzo E, Santos B, Freire R, Carballo JA, San-Segundo PA. Characterization of Pch2 localization determinants reveals a nucleolar-independent role in the meiotic recombination checkpoint. Chromosoma. 2019.

40. Joshi N, Barot A, Jamison C, Borner GV. Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet. 2009;5(7):e1000557. doi: 10.1371/journal.pgen.1000557 19629172

41. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Cell Biol. 2004;24(12):5534–47. doi: 10.1128/MCB.24.12.5534-5547.2004 15169913

42. Haruki H, Nishikawa J, Laemmli UK. The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell. 2008;31(6):925–32. doi: 10.1016/j.molcel.2008.07.020 18922474

43. Vincenten N, Kuhl LM, Lam I, Oke A, Kerr AR, Hochwagen A, et al. The kinetochore prevents centromere-proximal crossover recombination during meiosis. eLife. 2015;4.

44. Subramanian VV, Zhu X, Markowitz TE, Vale-Silva LA, San-Segundo PA, Hollingsworth NM, et al. Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes. Nat Comm. 2019;10(1):970.

45. Fan X, Moqtaderi Z, Jin Y, Zhang Y, Liu XS, Struhl K. Nucleosome depletion at yeast terminators is not intrinsic and can occur by a transcriptional mechanism linked to 3'-end formation. Proc Natl Acad Sci U S A. 2010;107(42):17945–50. doi: 10.1073/pnas.1012674107 20921369

46. Humphryes N, Leung WK, Argunhan B, Terentyev Y, Dvorackova M, Tsubouchi H. The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet. 2013;9(1):e1003194. doi: 10.1371/journal.pgen.1003194 23326245

47. Villar-Fernández MA CdSR, Pan D, Weir E, Sarembe A, Raina VB, Weir JR, Vader G. A meiosis-specific AAA+ assembly reveals repurposing of ORC during budding yeast gametogenesis. BioRxiv. 2019. doi: 10.1101/598128

48. Snyder M, Huang XY, Zhang JJ. The minichromosome maintenance proteins 2–7 (MCM2-7) are necessary for RNA polymerase II (Pol II)-mediated transcription. J Biol Chem. 2009;284(20):13466–72. doi: 10.1074/jbc.M809471200 19318354

49. Shor E, Warren CL, Tietjen J, Hou Z, Muller U, Alborelli I, et al. The origin recognition complex interacts with a subset of metabolic genes tightly linked to origins of replication. PLoS Genet. 2009;5(12):e1000755. doi: 10.1371/journal.pgen.1000755 19997491

50. Azvolinsky A, Giresi PG, Lieb JD, Zakian VA. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol Cell. 2009;34(6):722–34. doi: 10.1016/j.molcel.2009.05.022 19560424

51. Aparicio OM, Weinstein DM, Bell SP. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell. 1997;91(1):59–69. doi: 10.1016/s0092-8674(01)80009-x 9335335

52. Callebaut I, Courvalin JC, Mornon JP. The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett. 1999;446(1):189–93. doi: 10.1016/s0014-5793(99)00132-5 10100640

53. Muller P, Park S, Shor E, Huebert DJ, Warren CL, Ansari AZ, et al. The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev. 2010;24(13):1418–33. doi: 10.1101/gad.1906410 20595233

54. De Ioannes P LV, Kuang Z, Wang M, Boeke JD, Hochwagen A, Armache KJ. Structure and function of the Orc1 BAH-nucleosome complex. Nat Comm. 2019;Jul 1;10(1):2894.

55. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science. 2011;334(6058):977–82. doi: 10.1126/science.1210915 22096199

56. Weiner A, Hsieh TH, Appleboim A, Chen HV, Rahat A, Amit I, et al. High-resolution chromatin dynamics during a yeast stress response. Mol Cell. 2015;58(2):371–86. doi: 10.1016/j.molcel.2015.02.002 25801168

57. Smolle M, Workman JL. Transcription-associated histone modifications and cryptic transcription. Biochim. Biophys Acta, Gene Regul Mech. 2013;1829(1):84–97.

58. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, et al. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature. 2012;484(7392):115–9. doi: 10.1038/nature10956 22398447

59. Borner GV, Barot A, Kleckner N. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A. 2008;105(9):3327–32. doi: 10.1073/pnas.0711864105 18305165

60. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell. 2008;132(5):758–70. doi: 10.1016/j.cell.2008.01.035 18329363

61. Herruzo E, Ontoso D, Gonzalez-Arranz S, Cavero S, Lechuga A, San-Segundo PA. The Pch2 AAA+ ATPase promotes phosphorylation of the Hop1 meiotic checkpoint adaptor in response to synaptonemal complex defects. Nucleic Acids Res. 2016;44(16):7722–41. doi: 10.1093/nar/gkw506 27257060

62. Wood K, Tellier M, Murphy S. DOT1L and H3K79 Methylation in Transcription and Genomic Stability. Biomol. 2018;8(1):11.

63. Ditlev JA, Case LB, Rosen MK. Who's In and Who's Out-Compositional Control of Biomolecular Condensates. J Mol Biol. 2018;430(23):4666–84. doi: 10.1016/j.jmb.2018.08.003 30099028

64. Muller H, Scolari VF, Agier N, Piazza A, Thierry A, Mercy G, et al. Characterizing meiotic chromosomes' structure and pairing using a designer sequence optimized for Hi-C. Mol Syst Biol. 2018;14(7):e8293. doi: 10.15252/msb.20188293 30012718

65. Schalbetter SA, Fudenberg G, Baxter J, Pollard KS, Neale MJ. Principles of meiotic chromosome assembly revealed in S. cerevisiae. Nat Comm. 2019;10(1):4795.

66. Patel L, Kang R, Rosenberg SC, Qiu Y, Raviram R, Chee S, et al. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nat Struct Mol Biol. 2019;26(3):164–74. doi: 10.1038/s41594-019-0187-0 30778236

67. Wang Y, Wang H, Zhang Y, Du Z, Si W, Fan S, et al. Reprogramming of Meiotic Chromatin Architecture during Spermatogenesis. Mol Cell. 2019;73(3):547–61 e6. doi: 10.1016/j.molcel.2018.11.019 30735655

68. Alavattam KG, Maezawa S, Sakashita A, Khoury H, Barski A, Kaplan N, et al. Attenuated chromatin compartmentalization in meiosis and its maturation in sperm development. Nat Struct Mol Biol. 2019;26(3):175–84. doi: 10.1038/s41594-019-0189-y 30778237

69. Vara C, Paytuvi-Gallart A, Cuartero Y, Le Dily F, Garcia F, Salva-Castro J, et al. Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis. Cell Rep. 2019;28(2):352–67. doi: 10.1016/j.celrep.2019.06.037 31291573

70. Zhang L, Liang Z, Hutchinson J, Kleckner N. Crossover patterning by the beam-film model: analysis and implications. PLoS Genet. 2014;10(1):e1004042. doi: 10.1371/journal.pgen.1004042 24497834

71. Fujita T, Yuno M, Fujii H. enChIP systems using different CRISPR orthologues and epitope tags. BMC Res Notes. 2018;11(1):154. doi: 10.1186/s13104-018-3262-4 29482606

72. Silva RC, Dautel M, Di Genova BM, Amberg DC, Castilho BA, Sattlegger E. The Gcn2 Regulator Yih1 Interacts with the Cyclin Dependent Kinase Cdc28 and Promotes Cell Cycle Progression through G2/M in Budding Yeast. PloS One. 2015;10(7):e0131070. doi: 10.1371/journal.pone.0131070 26176233

73. Blitzblau HG, Hochwagen A. ATR/Mec1 prevents lethal meiotic recombination initiation on partially replicated chromosomes in budding yeast. eLife. 2013;2:e00844. doi: 10.7554/eLife.00844 24137535

74. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotech. 2011;29(1):24–6.

75. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30. doi: 10.1093/nar/28.1.27 10592173

76. Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44(W1):W160–5. doi: 10.1093/nar/gkw257 27079975

77. Collart MA, Struhl K. CDC39, an essential nuclear protein that negatively regulates transcription and differentially affects the constitutive and inducible HIS3 promoters. EMBO J. 1993;12(1):177–86. 8428577

Článek Duplication and divergence of the retrovirus restriction gene Fv1 in Mus caroli allows protection from multiple retroviruses

Článek Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase

Článek Steroid hormones regulate genome-wide epigenetic programming and gene transcription in human endometrial cells with marked aberrancies in endometriosis

Článek Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Článek Osteocalcin promotes bone mineralization but is not a hormone

Článek A conserved, N-terminal tyrosine signal directs Ras for inhibition by Rabex-5

Článek Integrins regulate epithelial cell shape by controlling the architecture and mechanical properties of basal actomyosin networks

Článek Cancer-associated mutations in the iron-sulfur domain of FANCJ affect G-quadruplex metabolism

Článek NRF2 loss recapitulates heritable impacts of paternal cigarette smoke exposure

Článek Pax6 organizes the anterior eye segment by guiding two distinct neural crest waves

Článek Transcriptomic stratification of late-onset Alzheimer's cases reveals novel genetic modifiers of disease pathology

Článek Alpha- and beta-adrenergic octopamine receptors in muscle and heart are required for Drosophila exercise adaptations