The Deacetylase Sir2 from the Yeast Clavispora lusitaniae Lacks the Evolutionarily Conserved Capacity to Generate Subtelomeric Heterochromatin

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Froyd, Cara A ^a   Kapoor, Shivali ^b   Dietrich, Fred ^a   Rusche, Laura N ^b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAVISPORA LUSITANIAE HST1 PROTEIN; CLAVISPORA LUSITANIAE NET1 PROTEIN; FUNGAL PROTEIN; HISTONE; REPETITIVE DNA; RIBOSOME DNA; SILENT INFORMATION REGULATOR PROTEIN 2; UNCLASSIFIED DRUG; CHROMATIN; HETEROCHROMATIN; HISTONE DEACETYLASE 3;

ADAPTATION; ARTICLE; CANDIDA ALBICANS; CHROMATIN STRUCTURE; CLAVISPORA LUSITANIAE; CONTROLLED STUDY; DEACETYLATION; FUNGAL GENE; FUNGAL STRAIN; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC CONSERVATION; HETEROCHROMATIN; HST1 GENE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLASTICITY; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIR2 GENE; STRAIN DIFFERENCE; TAXONOMIC RANK; TELOMERE; ACETYLATION; CHROMATIN; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SACCHAROMYCETALES;

ACETYLATION; CHROMATIN; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, FUNGAL; GROUP III HISTONE DEACETYLASES; HETEROCHROMATIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; TELOMERE;

EID: 84887264110     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003935     Document Type: Article

References (71)

1. Frye RA, (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273: 793-798.
2. Greiss S, Gartner A, (2009) Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation. Mol Cells 28: 407-415.
3. Imai S, Armstrong CM, Kaeberlein M, Guarente L, (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
4. Jackson MD, Denu JM, (2002) Structural identification of 2′- and 3′-O-acetyl-ADP ribose as novel metabolites derived from the Sir2 family of beta-NAD+-dependant histone/protein deacetylases. J Biol Chem 277: 18535-18544.
5. Guarente L, (2000) Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14: 1021-1026.
6. Lu SP, Lin SJ, (2010) Regulation of yeast sirtuins by NAD(+) metabolism and calorie restriction. Biochim Biophys Acta 1804: 1567-1575.
7. Donmez G, Guarente L, (2010) Aging and disease: connections to sirtuins. Aging Cell 9: 285-290.
8. Yu J, Auwerx J, (2009) The role of sirtuins in the control of metabolic homeostasis. Ann N Y Acad Sci 1173 (Suppl 1):: E10-19.
9. Ford E, Voit R, Liszt G, Magin C, Grummt I, et al. (2006) Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev 20: 1075-1080.
10. Grob A, Roussel P, Wright JE, McStay B, Hernandez-Verdun D, et al. (2009) Involvement of SIRT7 in resumption of rDNA transcription at the exit from mitosis. J Cell Sci 122: 489-498.
11. Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, et al. (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136: 62-74.
12. Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, et al. (2008) SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452: 492-496.
13. Freeman-Cook LL, Gomez EB, Spedale EJ, Marlett J, Forsburg SL, et al. (2005) Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+. Genetics 169: 1243-1260.
14. Hecht A, Strahl-Bolsinger S, Grunstein M, (1996) Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature 383: 92-96.
15. Gotta M, Strahl-Bolsinger S, Renauld H, Laroche T, Kennedy BK, et al. (1997) Localization of Sir2p: the nucleolus as a compartment for silent information regulators. EMBO J 16: 3243-3255.
16. 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.
17. Smith JS, Boeke JD, (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev 11: 241-254.
18. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I, (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 16: 4623-4635.
19. Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, et al. (2008) Epigenetic control of rDNA loci in response to intracellular energy status. Cell 133: 627-639.
20. Muth V, Nadaud S, Grummt I, Voit R, (2001) Acetylation of TAF(I)68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J 20: 1353-1362.
21. Zhou Y, Schmitz KM, Mayer C, Yuan X, Akhtar A, et al. (2009) Reversible acetylation of the chromatin remodelling complex NoRC is required for non-coding RNA-dependent silencing. Nat Cell Biol 11: 1010-1016.
22. Hickman MA, Froyd CA, Rusche LN, (2011) Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage. Eukaryot Cell 10: 1183-1192.
23. Froyd CA, Rusche LN, (2011) The duplicated deacetylases Sir2 and Hst1 subfunctionalized by acquiring complementary inactivating mutations. Mol Cell Biol 31: 3351-3365.
24. Hickman MA, Rusche LN, (2009) The Sir2-Sum1 complex represses transcription using both promoter-specific and long-range mechanisms to regulate cell identity and sexual cycle in the yeast Kluyveromyces lactis. PLoS Genet 5: e1000710.
25. Rusche LN, Kirchmaier AL, Rine J, (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72: 481-516.
26. Johnson LM, Kayne PS, Kahn ES, Grunstein M, (1990) Genetic evidence for an interaction between SIR3 and histone H4 in the repression of the silent mating loci in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 87: 6286-6290.
27. Kobayashi T, Ganley AR, (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581-1584.
28. Huang J, Moazed D, (2003) Association of the RENT complex with nontranscribed and coding regions of rDNA and a regional requirement for the replication fork block protein Fob1 in rDNA silencing. Genes Dev 17: 2162-2176.
29. Straight AF, Shou W, Dowd GJ, Turck CW, Deshaies RJ, et al. (1999) Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell 97: 245-256.
30. Huang J, Brito IL, Villen J, Gygi SP, Amon A, et al. (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 20: 2887-2901.
31. Kobayashi T, Horiuchi T, Tongaonkar P, Vu L, Nomura M, (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117: 441-453.
32. Byrne KP, Wolfe KH, (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15: 1456-1461.
33. Xie J, Pierce M, Gailus-Durner V, Wagner M, Winter E, et al. (1999) Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J 18: 6448-6454.
34. Bedalov A, Hirao M, Posakony J, Nelson M, Simon JA, (2003) NAD+-dependent deacetylase Hst1p controls biosynthesis and cellular NAD+ levels in Saccharomyces cerevisiae. Mol Cell Biol 23: 7044-7054.
35. McCord R, Pierce M, Xie J, Wonkatal S, Mickel C, et al. (2003) Rfm1, a novel tethering factor required to recruit the Hst1 histone deacetylase for repression of middle sporulation genes. Mol Cell Biol 23: 2009-2016.
36. Pierce M, Benjamin KR, Montano SP, Georgiadis MM, Winter E, et al. (2003) Sum1 and Ndt80 proteins compete for binding to middle sporulation element sequences that control meiotic gene expression. Mol Cell Biol 23: 4814-4825.
37. Astrom SU, Kegel A, Sjostrand JO, Rine J, (2000) Kluyveromyces lactis Sir2p regulates cation sensitivity and maintains a specialized chromatin structure at the cryptic alpha-locus. Genetics 156: 81-91.
38. Hickman MA, Rusche LN, (2007) Substitution as a mechanism for genetic robustness: the duplicated deacetylases Hst1p and Sir2p in Saccharomyces cerevisiae. PLoS Genetics 3: e126.
39. Shankaranarayana GD, Motamedi MR, Moazed D, Grewal SI, (2003) Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Curr Biol 13: 1240-1246.
40. Buscaino A, Lejeune E, Audergon P, Hamilton G, Pidoux A, et al. (2013) Distinct roles for Sir2 and RNAi in centromeric heterochromatin nucleation, spreading and maintenance. EMBO J 32: 1250-1264.
41. Wiren M, Silverstein RA, Sinha I, Walfridsson J, Lee HM, et al. (2005) Genomewide analysis of nucleosome density histone acetylation and HDAC function in fission yeast. EMBO J 24: 2906-2918.
42. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657-662.
43. Maguire SL, Oheigeartaigh SS, Byrne KP, Schroder MS, O'Gaora P, et al. (2013) Comparative genome analysis and gene finding in Candida species using CGOB. Mol Biol Evol 30: 1281-91.
44. Chen SC, Marriott D, Playford EG, Nguyen Q, Ellis D, et al. (2009) Candidaemia with uncommon Candida species: predisposing factors, outcome, antifungal susceptibility, and implications for management. Clin Microbiol Infect 15: 662-669.
45. Krcmery V, Barnes AJ, (2002) Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 50: 243-260.
46. Reedy JL, Floyd AM, Heitman J, (2009) Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19: 891-899.
47. Young LY, Lorenz MC, Heitman J, (2000) A STE12 homolog is required for mating but dispensable for filamentation in Candida lusitaniae. Genetics 155: 17-29.
48. Francois F, Noel T, Pepin R, Brulfert A, Chastin C, et al. (2001) Alternative identification test relying upon sexual reproductive abilities of Candida lusitaniae strains isolated from hospitalized patients. J Clin Microbiol 39: 3906-3914.
49. Lyons E, Freeling M, (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 53: 661-673.
50. Arnaud MB, Costanzo MC, Skrzypek MS, Shah P, Binkley G, et al. (2007) Sequence resources at the Candida Genome Database. Nucleic Acids Res 35: D452-456.
51. Fitzpatrick DA, O'Gaora P, Byrne KP, Butler G, (2010) Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser. BMC Genomics 11: 290.
52. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, et al. (2006) The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr Biol 16: 1280-1289.
53. Maas NL, Miller KM, DeFazio LG, Toczyski DP, (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109-119.
54. Conrad MN, Wright JH, Wolf AJ, Zakian VA, (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63: 739-750.
55. Longtine MS, Wilson NM, Petracek ME, Berman J, (1989) A yeast telomere binding activity binds to two related telomere sequence motifs and is indistinguishable from RAP1. Curr Genet 16: 225-239.
56. Luo K, Vega-Palas MA, Grunstein M, (2002) Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast. Genes Dev 16: 1528-1539.
57. Lustig AJ, Kurtz S, Shore D, (1990) Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science 250: 549-553.
58. Krauskopf A, Blackburn EH, (1996) Control of telomere growth by interactions of RAP1 with the most distal telomeric repeats. Nature 383: 354-357.
59. Li B, Oestreich S, Lange Td, (2000) Identification of human Rap1: Implications for telomere evolution. Cell 101: 471-483.
60. Longtine MS, Enomoto S, Finstad SL, Berman J, (1992) Yeast telomere repeat sequence (TRS) improves circular plasmid segregation, and TRS plasmid segregation involves the RAP1 gene product. Mol Cell Biol 12: 1997-2009.
61. Yu EY, Yen WF, Steinberg-Neifach O, Lue NF, (2010) Rap1 in Candida albicans: an unusual structural organization and a critical function in suppressing telomere recombination. Mol Cell Biol 30: 1254-1268.
62. Wyrick JJ, Holstege FC, Jennings EG, Causton HC, Shore D, et al. (1999) Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402: 418-421.
63. Kohler GA, White TC, Agabian N, (1997) Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J Bacteriol 179: 2331-2338.
64. Reuss O, Vik A, Kolter R, Morschhauser J, (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.
65. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
66. Lavoie H, Sellam A, Askew C, Nantel A, Whiteway M, (2008) A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9: 578.
67. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
68. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
69. Rusche LN, Rine J, (2001) Conversion of a gene-specific repressor to a regional silencer. Genes Dev 15: 955-967.
70. Schmitt ME, Brown TA, Trumpower BL, (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18: 3091-3092.
71. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.