The SAGA Histone Deubiquitinase Module Controls Yeast Replicative Lifespan via Sir2 Interaction

Cell Reports

Volumn 8, Issue 2, 2014, Pages 477-486

  McCormick, Mark A ^a,b   Mason, Amanda G ^c,d   Guyenet, Stephan J ^e   Dang, Weiwei ^f,g   Garza, Renee M ^d,h   Ting, Marc K ^a   Moller, Rick M ^e   Berger, Shelley L ^f   Kaeberlein, Matt ^e   Pillus, Lorraine ^e,h   LaSpada, Albert R ^c,d,e,i,j,k   Kennedy, Brian K ^a,b  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j UNIVERSITY OF CALIFORNIA   (United States)

^k UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ATAXIN 7; HISTONE DEACETYLASE; RIBOSOME DNA; SIRTUIN 2; TRANSCRIPTION FACTOR SAGA; DEUBIQUITINASE; GCN5 PROTEIN, S CEREVISIAE; HISTONE ACETYLTRANSFERASE; PROTEIN BINDING; PROTEINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SAGA COMPLEX, S CEREVISIAE; SGF73 PROTEIN, S CEREVISIAE; SILENT INFORMATION REGULATOR PROTEIN; SIR2 PROTEIN, S CEREVISIAE; TRANSACTIVATOR PROTEIN; UBP8 PROTEIN, S CEREVISIAE;

AGING; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; FUNGAL PHENOMENA AND FUNCTIONS; FUNGAL STRAIN; GCN5 GENE; GENE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE SILENCING; GENETIC RECOMBINATION; LIFE EXTENSION; LONGEVITY; NONHUMAN; OPEN READING FRAME; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SGF11 GENE; SGF73 GENE; TELOMERE; UBP8 GENE; YEAST REPLICATION; DNA RECOMBINATION; FUNGAL GENE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIFESPAN; PROTEIN INTERACTION; PROTEIN PURIFICATION; CELL PROLIFERATION; DNA REPLICATION; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CELL PROLIFERATION; DNA REPLICATION; ENDOPEPTIDASES; HISTONE ACETYLTRANSFERASES; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUIN 2; TRANS-ACTIVATORS;

EID: 84904810456     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.037     Document Type: Article

References (67)

1. Aparicio O.M., Billington B.L., Gottschling D.E. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell 1991, 66:1279-1287.
2. Armour S.M., Bennett E.J., Braun C.R., Zhang X.Y., McMahon S.B., Gygi S.P., Harper J.W., Sinclair D.A. A high-confidence interaction map identifies SIRT1 as a mediator of acetylation of USP22 and the SAGA coactivator complex. Mol. Cell. Biol. 2013, 33:1487-1502.
3. Belotserkovskaya R., Sterner D.E., Deng M., Sayre M.H., Lieberman P.M., Berger S.L. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Mol. Cell. Biol. 2000, 20:634-647.
4. Cai L., Sutter B.M., Li B., Tu B.P. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 2011, 42:426-437.
5. Cai L., McCormick M.A., Kennedy B.K., Tu B.P. Integration of multiple nutrient cues and regulation of lifespan by ribosomal transcription factor Ifh1. Cell Rep 2013, 4:1063-1071.
6. Dang W., Steffen K.K., Perry R., Dorsey J.A., Johnson F.B., Shilatifard A., Kaeberlein M., Kennedy B.K., Berger S.L. Histone H4 lysine 16 acetylation regulates cellular lifespan. Nature 2009, 459:802-807.
7. Daniel J.A., Torok M.S., Sun Z.W., Schieltz D., Allis C.D., Yates J.R., Grant P.A. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J.Biol. Chem. 2004, 279:1867-1871.
8. David G., Abbas N., Stevanin G., Dürr A., Yvert G., Cancel G., Weber C., Imbert G., Saudou F., Antoniou E., et al. Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nat. Genet. 1997, 17:65-70.
9. Defossez P.A., Prusty R., Kaeberlein M., Lin S.J., Ferrigno P., Silver P.A., Keil R.L., Guarente L. Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell 1999, 3:447-455.
10. Delaney J.R., Sutphin G.L., Dulken B., Sim S., Kim J.R., Robison B., Schleit J., Murakami C.J., Carr D., An E.H., et al. Sir2 deletion prevents lifespan extension in 32 long-lived mutants. Aging Cell 2011, 10:1089-1091.
11. Downey M., Knight B., Vashisht A.A., Seller C.A., Wohlschlegel J.A., Shore D., Toczyski D.P. Gcn5 and sirtuins regulate acetylation of the ribosomal protein transcription factor Ifh1. Curr. Biol. 2013, 23:1638-1648.
12. Emre N.C., Ingvarsdottir K., Wyce A., Wood A., Krogan N.J., Henry K.W., Li K., Marmorstein R., Greenblatt J.F., Shilatifard A., Berger S.L. Maintenance of low histone ubiquitylation by Ubp10 correlates with telomere-proximal Sir2 association and gene silencing. Mol. Cell 2005, 17:585-594.
13. Fourel G., Revardel E., Koering C.E., Gilson E. Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J. 1999, 18:2522-2537.
14. Garcia S.N., Pillus L. A unique class of conditional sir2 mutants displays distinct silencing defects in Saccharomyces cerevisiae. Genetics 2002, 162:721-736.
15. Gottlieb S., Esposito R.E. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 1989, 56:771-776.
16. Guarente L. Sirtuins, aging, and metabolism. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:81-90.
17. Helmlinger D., Hardy S., Sasorith S., Klein F., Robert F., Weber C., Miguet L., Potier N., Van-Dorsselaer A., Wurtz J.M., et al. Ataxin-7 is a subunit of GCN5 histone acetyltransferase-containing complexes. Hum. Mol. Genet. 2004, 13:1257-1265.
18. Henry K.W., Wyce A., Lo W.S., Duggan L.J., Emre N.C., Kao C.F., Pillus L., Shilatifard A., Osley M.A., Berger S.L. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 2003, 17:2648-2663.
19. Holmberg M., Duyckaerts C., Dürr A., Cancel G., Gourfinkel-An I., Damier P., Faucheux B., Trottier Y., Hirsch E.C., Agid Y., Brice A. Spinocerebellar ataxia type 7 (SCA7): a neurodegenerative disorder with neuronal intranuclear inclusions. Hum. Mol. Genet. 1998, 7:913-918.
20. Jacobson S., Pillus L. The SAGA subunit Ada2 functions in transcriptional silencing. Mol. Cell. Biol. 2009, 29:6033-6045.
21. Jazwinski S.M. Rtg2 protein: at the nexus of yeast longevity and aging. FEMS Yeast Res. 2005, 5:1253-1259.
22. Kaeberlein M., McVey M., Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 1999, 13:2570-2580.
23. Kaeberlein M., Kirkland K.T., Fields S., Kennedy B.K. Sir2-independent life span extension by calorie restriction in yeast. PLoS Biol. 2004, 2:E296.
24. Kaeberlein M., Kirkland K.T., Fields S., Kennedy B.K. Genes determining yeast replicative life span in a long-lived genetic background. Mech. Ageing Dev. 2005, 126:491-504.
25. Kaeberlein M., Powers R.W., Steffen K.K., Westman E.A., Hu D., Dang N., Kerr E.O., Kirkland K.T., Fields S., Kennedy B.K. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 2005, 310:1193-1196.
26. Kamata K., Hatanaka A., Goswami G., Shinmyozu K., Nakayama J., Urano T., Hatashita M., Uchida H., Oki M. C-terminus of the Sgf73 subunit of SAGA and SLIK is important for retention in the larger complex and for heterochromatin boundary function. Genes Cells 2013, 18:823-837.
27. Kaplan E.L., Meier P. Nonparametric estimation from incomplete observations. J.Am. Stat. Assoc. 1958, 53:457-481.
28. Kaytor M.D., Duvick L.A., Skinner P.J., Koob M.D., Ranum L.P., Orr H.T. Nuclear localization of the spinocerebellar ataxia type 7 protein, ataxin-7. Hum. Mol. Genet. 1999, 8:1657-1664.
29. Kennedy B.K., Austriaco N.R., Zhang J., Guarente L. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 1995, 80:485-496.
30. Köhler A., Schneider M., Cabal G.G., Nehrbass U., Hurt E. Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat. Cell Biol. 2008, 10:707-715.
31. Kwan E.X., Foss E.J., Tsuchiyama S., Alvino G.M., Kruglyak L., Kaeberlein M., Raghuraman M.K., Brewer B.J., Kennedy B.K., Bedalov A. A natural polymorphism in rDNA replication origins links origin activation with calorie restriction and lifespan. PLoS Genet. 2013, 9:e1003329.
32. La Spada A.R., Taylor J.P. Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat. Rev. Genet. 2010, 11:247-258.
33. La Spada A.R., Fu Y.H., Sopher B.L., Libby R.T., Wang X., Li L.Y., Einum D.D., Huang J., Possin D.E., Smith A.C., et al. Polyglutamine-expanded ataxin-7 antagonizes CRX function and induces cone-rod dystrophy in a mouse model of SCA7. Neuron 2001, 31:913-927.
34. Lebre A.S., Brice A. Spinocerebellar ataxia 7 (SCA7). Cytogenet. Genome Res. 2003, 100:154-163.
35. Lee K.K., Swanson S.K., Florens L., Washburn M.P., Workman J.L. Yeast Sgf73/Ataxin-7 serves to anchor the deubiquitination module into both SAGA and Slik(SALSA) HAT complexes. Epigenetics Chromatin 2009, 2:2.
36. Lin Z., Yang H., Kong Q., Li J., Lee S.M., Gao B., Dong H., Wei J., Song J., Zhang D.D., Fang D. USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol. Cell 2012, 46:484-494.
37. Mal A.K. Histone methyltransferase Suv39h1 represses MyoD-stimulated myogenic differentiation. EMBO J. 2006, 25:3323-3334.
38. Martinez E., Palhan V.B., Tjernberg A., Lymar E.S., Gamper A.M., Kundu T.K., Chait B.T., Roeder R.G. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors invivo. Mol. Cell. Biol. 2001, 21:6782-6795.
39. Mehta R., Chandler-Brown D., Ramos F.J., Shamieh L.S., Kaeberlein M. Regulation of mRNA translation as a conserved mechanism of longevity control. Adv. Exp. Med. Biol. 2010, 694:14-29.
40. Mortimer R.K., Johnston J.R. Life span of individual yeast cells. Nature 1959, 183:1751-1752.
41. Mushegian A.R., Vishnivetskiy S.A., Gurevich V.V. Conserved phosphoprotein interaction motif is functionally interchangeable between ataxin-7 and arrestins. Biochemistry 2000, 39:6809-6813.
42. Oki M., Valenzuela L., Chiba T., Ito T., Kamakaka R.T. Barrier proteins remodel and modify chromatin to restrict silenced domains. Mol. Cell. Biol. 2004, 24:1956-1967.
43. Palhan V.B., Chen S., Peng G.H., Tjernberg A., Gamper A.M., Fan Y., Chait B.T., La Spada A.R., Roeder R.G. Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc. Natl. Acad. Sci. USA 2005, 102:8472-8477.
44. Pryde F.E., Louis E.J. Limitations of silencing at native yeast telomeres. EMBO J. 1999, 18:2538-2550.
45. Rossmann M.P., Luo W., Tsaponina O., Chabes A., Stillman B. A common telomeric gene silencing assay is affected by nucleotide metabolism. Mol. Cell 2011, 42:127-136.
46. Scheel H., Tomiuk S., Hofmann K. Elucidation of ataxin-3 and ataxin-7 function by integrative bioinformatics. Hum. Mol. Genet. 2003, 12:2845-2852.
47. Schulze J.M., Hentrich T., Nakanishi S., Gupta A., Emberly E., Shilatifard A., Kobor M.S. Splitting the task: Ubp8 and Ubp10 deubiquitinate different cellular pools of H2BK123. Genes Dev. 2011, 25:2242-2247.
48. Sinclair D.A., Guarente L. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 1997, 91:1033-1042.
49. Smith J.S., Boeke J.D. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 1997, 11:241-254.
50. Smith E.D., Tsuchiya M., Fox L.A., Dang N., Hu D., Kerr E.O., Johnston E.D., Tchao B.N., Pak D.N., Welton K.L., et al. Quantitative evidence for conserved longevity pathways between divergent eukaryotic species. Genome Res. 2008, 18:564-570.
51. Smolle M., Venkatesh S., Gogol M.M., Li H., Zhang Y., Florens L., Washburn M.P., Workman J.L. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 2012, 19:884-892.
52. Spedale G., Mischerikow N., Heck A.J., Timmers H.T., Pijnappel W.W. Identification of Pep4p as the protease responsible for formation of the SAGA-related SLIK protein complex. J.Biol. Chem. 2010, 285:22793-22799.
53. Stanfel M.N., Shamieh L.S., Kaeberlein M., Kennedy B.K. The TOR pathway comes of age. Biochim. Biophys. Acta 2009, 1790:1067-1074.
54. Steffen K.K., MacKay V.L., Kerr E.O., Tsuchiya M., Hu D., Fox L.A., Dang N., Johnston E.D., Oakes J.A., Tchao B.N., et al. Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4. Cell 2008, 133:292-302.
55. Steffen K.K., Kennedy B.K., Kaeberlein M. Measuring replicative life span in the budding yeast. J.Vis. Exp. 2009.
56. Steinkraus K.A., Kaeberlein M., Kennedy B.K. Replicative aging in yeast: the means to the end. Annu. Rev. Cell Dev. Biol. 2008, 24:29-54.
57. Sutphin G.L., Olsen B.A., Kennedy B.K., Kaeberlein M. Genome-wide analysis of yeast aging. Subcell. Biochem. 2012, 57:251-289.
58. Trujillo K.M., Osley M.A. A role for H2B ubiquitylation in DNA replication. Mol. Cell 2012, 48:734-746.
59. Vega-Palas M.A., Venditti S., Di Mauro E. Telomeric transcriptional silencing in a natural context. Nat. Genet. 1997, 15:232-233.
60. Vega-Palas M.A., Martín-Figueroa E., Florencio F.J. Telomeric silencing of a natural subtelomeric gene. Mol. Gen. Genet. 2000, 263:287-291.
61. Wilcoxon F. Individual comparisons of grouped data by ranking methods. J.Econ. Entomol. 1946, 39:269.
62. Winzeler E.A., Shoemaker D.D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J.D., Bussey H., et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999, 285:901-906.
63. Wyrick J.J., Holstege F.C., Jennings E.G., Causton H.C., Shore D., Grunstein M., Lander E.S., Young R.A. Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 1999, 402:418-421.
64. Xu F., Zhang Q., Zhang K., Xie W., Grunstein M. Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol. Cell 2007, 27:890-900.
65. Zhang X.Y., Varthi M., Sykes S.M., Phillips C., Warzecha C., Zhu W., Wyce A., Thorne A.W., Berger S.L., McMahon S.B. The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol. Cell 2008, 29:102-111.
66. Zhao Y., Lang G., Ito S., Bonnet J., Metzger E., Sawatsubashi S., Suzuki E., Le Guezennec X., Stunnenberg H.G., Krasnov A., et al. A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol. Cell 2008, 29:92-101.
67. Zoghbi H.Y., Orr H.T. Pathogenic mechanisms of a polyglutamine-mediated neurodegenerative disease, spinocerebellar ataxia type 1. J.Biol. Chem. 2009, 284:7425-7429.