Role of SAGA in the asymmetric segregation of DNA circles during yeast ageing

eLife

Volumn 2014, Issue 3, 2014, Pages 1-33

  Denoth Lippuner, Annina ^a   Krzyzanowski, Marek Konrad ^a   Stober, Catherine ^a   Barral, Yves ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DNA; EXTRACHROMOSOMAL DNA; NUCLEOPORIN; RIBOSOME DNA; TRANSCRIPTION FACTOR SAGA;

ARTICLE; CELL AGING; CELL DIVISION; CENTROMERE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME SEGREGATION; COLONY FORMATION; DAUGHTER CELL; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MICROFLUIDICS; NONHUMAN; NUCLEAR PORE COMPLEX; PEDIGREE ANALYSIS; POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TIME-LAPSE VIDEO MICROSCOPY; YEAST;

EUKARYOTA;

EID: 84922017548     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03790.001     Document Type: Article

References (62)

1. Boettcher B, Marquez-Lago TT, Bayer M, Weiss EL, Barral Y. 2012. Nuclear envelope morphology constrains diffusion and promotes asymmetric protein segregation in closed mitosis. The Journal of Cell Biology 197: 921-937. doi: 10.1083/jcb.201112117.
2. Bonnet J, Wang CY, Baptista T, Vincent SD, Hsiao WC, Stierle M, Kao CF, Tora L, Devys D. 2014. The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription. Genes & Development 28:1999-2012. doi: 10.1101/gad.250225.114.
3. Bupp JM, Martin AE, Stensrud ES, Jaspersen SL. 2007. Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. The Journal of Cell Biology 179:845-854. doi: 10.1083/jcb.200706040.
4. Burtner CR, Kennedy BK. 2010. Progeria syndromes and ageing: what is the connection? Nature Reviews Molecular Cell Biology 11:567-578. doi: 10.1038/nrm2944.
5. Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin JC, Hurt EC, Nehrbass U. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441:770-773. doi: 10.1038/nature04752.
6. Chadrin A, Hess B, San Roman M, Gatti X, Lombard B, Loew D, Barral Y, Palancade B, Doye V. 2010. Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. The Journal of Cell Biology 189:795-811. doi: 10.1083/jcb.200910043.
7. Chymkowitch P, Eldholm V, Lorenz S, Zimmermann C, Lindvall JM, Bjoras M, Meza-Zepeda LA, Enserink JM. 2012. Cdc28 kinase activity regulates the basal transcription machinery at a subset of genes. Proceedings of the National Academy of Sciences of USA 109:10450-10455. doi: 10.1073/pnas.1200067109.
8. Clay L, Caudron F, Denoth-Lippuner A, Boettcher B, Buvelot Frei S, Snapp EL, Barral Y. 2014. A sphingolipid- dependent diffusion barrier confines ER stress to the yeast mother cell. ELife 3 e01883. doi: 10.7554/eLife.01883.
9. Cohen S, Agmon N, Sobol O, Segal D. 2010. Extrachromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mobile DNA 1:11. doi: 10.1186/1759-8753-1-11.
10. Cohen S, Segal D. 2009. Extrachromosomal circular DNA in eukaryotes: possible involvement in the plasticity of tandem repeats. Cytogenetic and Genome Research 124:327-338. doi: 10.1159/000218136.
11. Cohen S, Yacobi K, Segal D. 2003. Extrachromosomal circular DNA of tandemly repeated genomic sequences in Drosophila. Genome Research 13:1133-1145. doi: 10.1101/gr.907603.
12. Colombi P, Webster BM, Frohlich F, Lusk CP. 2013. The transmission of nuclear pore complexes to daughter cells requires a cytoplasmic pool of Nsp1. The Journal of Cell Biology 203:215-232. doi: 10.1083/jcb.201305115.
13. Cook CE, Hochstrasser M, Kerscher O. 2009. The SUMO-targeted ubiquitin ligase subunit Slx5 resides in nuclear foci and at sites of DNA breaks. Cell Cycle 8:1080-1089. doi: 10.4161/cc.8.7.8123.
14. Defossez PA, Prusty R, Kaeberlein M, Lin SJ, Ferrigno P, Silver PA, Keil RL, Guarente L. 1999. Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Molecular Cell 3:447-455. doi: 10.1016/S1097-2765(00)80472-4.
15. Denoth Lippuner A, Julou T, Barral Y. 2014. Budding yeast as a model organism to study the effects of age. FEMS Microbiology Reviews 38:300-325. doi: 10.1111/1574-6976.12060.
16. Dilworth DJ, Suprapto A, Padovan JC, Chait BT, Wozniak RW, Rout MP, Aitchison JD. 2001. Nup2p dynamically associates with the distal regions of the yeast nuclear pore complex. The Journal of Cell Biology 153: 1465-1478. doi: 10.1083/jcb.153.7.1465.
17. Espinosa MC, Rehman MA, Chisamore-Robert P, Jeffery D, Yankulov K. 2010. GCN5 is a positive regulator of origins of DNA replication in Saccharomyces cerevisiae. PLOS ONE 5:e8964. doi: 10.1371/journal.pone.0008964.
18. Falcon AA, Aris JP. 2003. Plasmid accumulation reduces life span in Saccharomyces cerevisiae. The Journal of Biological Chemistry 278:41607-41617. doi: 10.1074/jbc.M307025200.
19. Fischer T, Strasser K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. The EMBO Journal 21:5843-5852. doi: 10.1093/emboj/cdf590.
20. Futcher AB, Cox BS. 1984. Copy number and the stability of 2-micron circle-based artificial plasmids of Saccharomyces cerevisiae. Journal of Bacteriology 157:283-290.
21. Gaubatz JW. 1990. Extrachromosomal circular DNAs and genomic sequence plasticity in eukaryotic cells. Mutation Research 237:271-292. doi: 10.1016/0921-8734(90)90009-G.
22. Gehlen LR, Nagai S, Shimada K, Meister P, Taddei A, Gasser SM. 2011. Nuclear geometry and rapid mitosis ensure asymmetric episome segregation in yeast. Current Biology 21:25-33. doi: 10.1016/j.cub.2010.12.016.
23. Gillespie CS, Proctor CJ, Boys RJ, Shanley DP, Wilkinson DJ, Kirkwood TB. 2004. A mathematical model of ageing in yeast. Journal of Theoretical Biology 229:189-196. doi: 10.1016/j.jtbi.2004.03.015.
24. Goshima G, Yanagida M. 2000. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell 100:619-633. doi: 10.1016/S0092-8674(00)80699-6.
25. Gotta M, Laroche T, Formenton A, Maillet L, Scherthan H, Gasser SM. 1996. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. The Journal of Cell Biology 134:1349-1363. doi: 10.1083/jcb.134.6.1349.
26. Gottlieb S, Esposito RE. 1989. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56:771-776. doi: 10.1016/0092-8674(89)90681-8.
27. Green EM, Jiang Y, Joyner R, Weis K. 2012. A negative feedback loop at the nuclear periphery regulates GAL gene expression. Molecular Biology of the Cell 23:1367-1375. doi: 10.1091/mbc.E11-06-0547.
28. Gruber S, Arumugam P, Katou Y, Kuglitsch D, Helmhart W, Shirahige K, Nasmyth K. 2006. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127:523-537. doi: 10.1016/j.cell.2006.08.048.
29. Grund SE, Fischer T, Cabal GG, Antunez O, Perez-Ortin JE, Hurt E. 2008. The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. The Journal of Cell Biology 182:897-910. doi: 10.1083/jcb.200803098.
30. Heyer WD. 2004. Recombination: Holliday junction resolution and crossover formation. Current Biology 14:R56-R58. doi: 10.1016/j.cub.2003.12.043.
31. Huberts DH, Sik Lee S, Gonzales J, Janssens GE, Vizcarra IA, Heinemann M. 2013. Construction and use of a microfluidic dissection platform for long-term imaging of cellular processes in budding yeast. Nature Protocols 8:1019-1027. doi: 10.1038/nprot.2013.060.
32. Hyman BC, Cramer JH, Rownd RH. 1982. Properties of a Saccharomyces cerevisiae mtDNA segment conferring high-frequency yeast transformation. Proceedings of the National Academy of Sciences of USA 79:1578-1582. doi: 10.1073/pnas.79.5.1578.
33. Jacobson S, Pillus L. 2009. The SAGA subunit Ada2 functions in transcriptional silencing. Molecular and Cellular Biology 29:6033-6045. doi: 10.1128/MCB.00542-09.
34. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21:947-962. doi: 10.1002/yea.1142.
35. Jaspersen SL, Ghosh S. 2012. Nuclear envelope insertion of spindle pole bodies and nuclear pore complexes. Nucleus 3:226-236. doi: 10.4161/nucl.20148.
36. Kaeberlein M, McVey M, Guarente L. 1999. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes & Development 13:2570-2580. doi: 10.1101/gad.13.19.2570.
37. Khmelinskii A, Keller PJ, Lorenz H, Schiebel E, Knop M. 2010. Segregation of yeast nuclear pores. Nature 466:E1. doi: 10.1038/nature09255.
38. Khmelinskii A, Meurer M, Knop M, Schiebel E. 2011. Artificial tethering to nuclear pores promotes partitioning of extrachromosomal DNA during yeast asymmetric cell division. Current Biology 21:R17-R18. doi: 10.1016/j.cub.2010.11.034.
39. Lee SS, Avalos Vizcarra I, Huberts DH, Lee LP, Heinemann M. 2012. Whole lifespan microscopic observation of budding yeast aging through a microfluidic dissection platform. Proceedings of the National Academy of Sciences of USA 109:4916-4920. doi: 10.1073/pnas.1113505109.
40. Lindstrom DL, Gottschling DE. 2009. The mother enrichment program: a genetic system for facile replicative life span analysis in Saccharomyces cerevisiae. Genetics 183:413-422, 411SI-413SI. doi: 10.1534/genetics.109.106229.
41. Lindstrom DL, Leverich CK, Henderson KA, Gottschling DE. 2011. Replicative age induces mitotic recombination in the ribosomal RNA gene cluster of Saccharomyces cerevisiae. PLOS Genetics 7:e1002015. doi: 10.1371/journal.pgen.1002015.
42. Luedeke C, Frei SB, Sbalzarini I, Schwarz H, Spang A, Barral Y. 2005. Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth. The Journal of Cell Biology 169:897-908. doi: 10.1083/jcb.200412143.
43. Luthra R, Kerr SC, Harreman MT, Apponi LH, Fasken MB, Ramineni S, Chaurasia S, Valentini SR, Corbett AH. 2007. Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. The Journal of Biological Chemistry 282:3042-3049. doi: 10.1074/jbc.M608741200.
44. Makio T, Lapetina DL, Wozniak RW. 2013. Inheritance of yeast nuclear pore complexes requires the Nsp1p subcomplex. The Journal of Cell Biology 203:187-196. doi: 10.1083/jcb.201304047.
45. McCormick MA, Mason AG, Guyenet SJ, Dang W, Garza RM, Ting MK, Moller RM, Berger SL, Kaeberlein M, Pillus L, La Spada AR, Kennedy BK. 2014. The SAGA histone Deubiquitinase Module controls yeast replicative lifespan via Sir2 interaction. Cell Reports 8:477-486. doi: 10.1016/j.celrep.2014.06.037.
46. Megee PC, Koshland D. 1999. A functional assay for centromere-associated sister chromatid cohesion. Science 285:254-257. doi: 10.1126/science.285.5425.254.
47. Menendez-Benito V, van Deventer SJ, Jimenez-Garcia V, Roy-Luzarraga M, van Leeuwen F, Neefjes J. 2013. Spatiotemporal analysis of organelle and macromolecular complex inheritance. Proceedings of the National Academy of Sciences of USA 110:175-180. doi: 10.1073/pnas.1207424110.
48. Mortimer RK, Johnston JR. 1959. Life span of individual yeast cells. Nature 183:1751-1752. doi: 10.1038/1831751a0.
49. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103-118.
50. Ohtsuki K, Kasahara K, Shirahige K, Kokubo T. 2010. Genome-wide localization analysis of a complete set of Tafs reveals a specific effect of the taf1 mutation on Taf2 occupancy and provides indirect evidence for different TFIID conformations at different promoters. Nucleic Acids Research 38:1805-1820. doi: 10.1093/nar/gkp1172.
51. Ouellet J, Barral Y. 2012. Organelle segregation during mitosis: lessons from asymmetrically dividing cells. The Journal of Cell Biology 196:305-313. doi: 10.1083/jcb.201102078.
52. Pascual-Garcia P, Rodriguez-Navarro S. 2009. A tale of coupling, Sus1 function in transcription and mRNA export. RNA Biology 6:141-144. doi: 10.4161/rna.6.2.7793.
53. Rodriguez-Navarro S, Fischer T, Luo MJ, Antunez O, Brettschneider S, Lechner J, Perez-Ortin JE, Reed R, Hurt E. 2004. Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116:75-86. doi: 10.1016/S0092-8674(03)01025-0.
54. Scaffidi P, Misteli T. 2006. Lamin A-dependent nuclear defects in human aging. Science 312:1059-1063. doi: 10.1126/science.1127168.
55. Schleit J, Johnson SC, Bennett CF, Simko M, Trongtham N, Castanza A, Hsieh EJ, Moller RM, Wasko BM, Delaney JR, Sutphin GL, Carr D, Murakami CJ, Tocchi A, Xian B, Chen W, Yu T, Goswami S, Higgins S, Holmberg M, Jeong KS, Kim JR, Klum S, Liao E, Lin MS, Lo W, Miller H, Olsen B, Peng ZJ, Pollard T, Pradeep P, Pruett D, Rai D, Ros V, Singh M, Spector BL, Vander Wende H, An EH, Fletcher M, Jelic M, Rabinovitch PS, MacCoss MJ, Han JD, Kennedy BK, Kaeberlein M. 2013. Molecular mechanisms underlying genotype-dependent responses to dietary restriction. Aging Cell 12:1050-1061. doi: 10.1111/acel.12130.
56. Sharma S, Doherty KM, Brosh RM. 2006. Mechanisms of RecQ helicases in pathways of DNA metabolism and maintenance of genomic stability. The Biochemical Journal 398:319-337. doi: 10.1042/BJ20060450.
57. Shcheprova Z, Baldi S, Frei SB, Gonnet G, Barral Y. 2008. A mechanism for asymmetric segregation of age during yeast budding. Nature 454:728-734. doi: 10.1038/nature07212.
58. Shibata Y, Kumar P, Layer R, Willcox S, Gagan JR, Griffith JD, Dutta A. 2012. Extrachromosomal microDNAs and chromosomal microdeletions in normal tissues. Science 336:82-86. doi: 10.1126/science.1213307.
59. Sinclair DA, Guarente L. 1997. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91:1033-1042. doi: 10.1016/S0092-8674(00)80493-6.
60. Steinberg G, Schuster M, Theisen U, Kilaru S, Forge A, Martin-Urdiroz M. 2012. Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport. The Journal of Cell Biology 198:343-355. doi: 10.1083/jcb.201201087.
61. Vinciguerra P, Stutz F. 2004. mRNA export: an assembly line from genes to nuclear pores. Current Opinion in Cell Biology 16:285-292. doi: 10.1016/j.ceb.2004.03.013.
62. Wang L, Liu L, Berger SL. 1998. Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo. Genes & Development 12:640-653. doi: 10.1101/gad.12.5.640.