A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation

Molecular Microbiology

Volumn 63, Issue 3, 2007, Pages 724-736

  Alsford, Sam ^a   Kawahara, Taemi ^a   Isamah, Cyril ^a   Horn, David ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GLYCOPROTEIN; MITOCHONDRIAL PROTEIN; NUCLEAR PROTEIN; POL PROTEIN; RNA POLYMERASE; SILENT INFORMATION REGULATOR PROTEIN 2; SIRTUIN;

ANTIGENIC VARIATION; ARTICLE; BLOOD FLOW; CELL NUCLEUS MEMBRANE; DNA REPAIR; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TELOMERE; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENIC VARIATION; DNA REPAIR; GENE SILENCING; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; SIRTUINS; TELOMERE; TRYPANOSOMA BRUCEI BRUCEI;

MAMMALIA; PROTOZOA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 33846194528     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05553.x     Document Type: Article

References (51)

1. Alsford, S., Kawahara, T., Glover, L., and Horn, D. (2005) Tagging a T. brucei RRNA locus improves stable transfection efficiency and circumvents inducible expression position effects. Mol Biochem Parasitol 144: 142-148.
2. Bell, S.D., Botting, C.H., Wardleworth, B.N., Jackson, S.P., and White, M.F. (2002) The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science 296: 148-151.
3. Bitterman, K.J., Anderson, R.M., Cohen, H.Y., Latorre-Esteves, M., and Sinclair, D.A. (2002) Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J Biol Chem 277: 45099-45107.
4. Blander, G., and Guarente, L. (2004) The sir2 family of protein deacetylases. Annu Rev Biochem 73: 417-435.
5. Chang, J.H., Kim, H.C., Hwang, K.Y., Lee, J.W., Jackson, S.P., Bell, S.D., and Cho, Y. (2002) Structural basis for the NAD-dependent deacetylase mechanism of Sir2. J Biol Chem 277: 34489-34498.
6. Chen, X.J., and Clark Walker, G.D. (1994) sir2 mutants of Kluyveromyces lactis are hypersensitive to DNA-targeting drugs. Mol Cell Biol 14: 4501-4508.
7. Cockell, M.M., Perrod, S., and Gasser, S.M. (2000) Analysis of Sir2p domains required for rDNA and telomeric silencing in Saccharomyces cerevisiae. Genetics 154: 1069-1083.
8. Figueiredo, L., and Scherf, A. (2005) Plasmodium telomeres and telomerase: the usual actors in an unusual scenario. Chromosome Res 13: 517-524.
9. Frye, R.A. (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Comm 273: 793-798.
10. Garcia-Salcedo, J.A., Gijon, P., Nolan, D.P., Tebabi, P., and Pays, E. (2003) A chromosomal SIR2 homologue with both histone NAD-dependent ADP-ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei. EMBO J 22: 5851-5862.
11. Glover, L., and Horn, D. (2006) Repression of polymerase I-mediated gene expression at Trypanosoma brucei telomeres. EMBO Rep 7: 93-99.
12. Gottlieb, S., and Esposito, R.E. (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56: 771-776.
13. Haigis, M.C., Mostoslavsky, R., Haigis, K.M., Fahie, K., Christodoulou, D.C., Murphy, A.J., et al. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic b cells. Cell 126: 941-954.
14. Hallows, W.C., Lee, S., and Denu, J.M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103: 10230-10235.
15. Hausler, T., Stierhof, Y.D., Blattner, J., and Clayton, C. (1997) Conservation of mitochondrial targeting sequence function in mitochondrial and hydrogenosomal proteins from the early-branching eukaryotes Crithidia, Trypanosoma and Trichomonas. Eur J Cell Biol 73: 240-251.
16. Hecht, A., Strahl-Bolsinger, S., and Grunstein, M. (1996) Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature 383: 92-96.
17. Holmes, S.G., Rose, A.B., Steuerle, K., Saez, E., Sayegh, S., Lee, Y.M., and Broach, J.R. (1997) Hyperactivation of the silencing proteins, Sir2p and Sir3p, causes chromosome loss. Genetics 145: 605-614.
18. Horn, D., and Cross, G.A. (1997a) Analysis of Trypanosoma brucei vsg expression site switching in vitro. Mol Biochem Parasitol 84: 189-201.
19. Horn, D., and Cross, G.A. (1997b) Position-dependent and promoter-specific regulation of gene expression in Trypanosoma brucei. EMBO J 16: 7422-7431.
20. Horn, D., and Barry, J.D. (2005) The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosome Res 13: 525-533.
21. Imai, S., Armstrong, C.M., Kaeberlein, M., and Guarente, L. (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
22. Ingram, A.K., and Horn, D. (2002) Histone deacetylases in Trypanosoma brucei: two are essential and another is required for normal cell cycle progression. Mol Microbiol 45: 89-97.
23. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
24. Janzen, C.J., Fernandez, J.P., Deng, H., Diaz, R., Hake, S.B., and Cross, G.A. (2006) Unusual histone modifications in Trypanosoma brucei. FEBS Lett 580: 2306-2310.
25. Liszt, G., Ford, E., Kurtev, M., and Guarente, L. (2005) Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem 280: 21313-21320.
26. Longtine, M.S., Enomoto, S., Finstad, S.L., and Berman, J. (1993) Telomere-mediated plasmid segregation in Saccharomyces cerevisiae involves gene products required for transcriptional repression at silencers and telomeres. Genetics 133: 171-182.
27. Luo, J., Nikolaev, A.Y., Imai, S., Chen, D., Su, F., Shiloh, A., et al. (2001) Negative control of p53 by Sir2 promotes cell survival under stress. Cell 107: 137-148.
28. Martin, S.G., Laroche, T., Suka, N., Grunstein, M., and Gasser, S.M. (1999) Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell 97: 621-633.
29. Michishita, E., Park, J.Y., Burneskis, J.M., Barrett, J.C., and Horikawa, I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 16: 4623-4635.
30. Min, J., Landry, J., Sternglanz, R., and Xu, R.M. (2001) Crystal structure of a SIR2 homolog-NAD complex. Cell 105: 269-279.
31. Mostoslavsky, R., Chua, K.F., Lombard, D.B., Pang, W.W., Fischer, M.R., Gellon, L., et al. (2006) Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124: 315-329.
32. Muth, V., Nadaud, S., Grummt, I., and Voit, R. (2001) Acetylation of TAFI68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J 20: 1353-1362.
33. +-dependent tubulin deacetylase. Mol Cell 11: 437-444.
34. +-dependent Sir2p histone deacetylase is a negative regulator of chromosomal DNA replication. Genes Dev 18: 769-781.
35. Perez-Martin, J., Uria, J.A., and Johnson, A.D. (1999) Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J 18: 2580-2592.
36. Perrod, S., Cockell, M.M., Laroche, T., Renauld, H., Ducrest, A., Bonnard, C., and Gasser, M. (2001) A cytosolic NAD-dependent deacetylase, Hst2p, can modulate nucleolar and telomeric silencing in yeast. EMBO J 20: 197-209.
37. Proudfoot, C., and McCulloch, R. (2005) Distinct roles for two RAD51-related genes in Trypanosoma brucei antigenic variation. Nucleic Acids Res 33: 6906-6919.
38. Rusche, L.N., Kirchmaier, A.L., and Rine, J. (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72: 481-516.
39. Sasse, R., and Gull, K. (1988) Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei. J Cell Sci 90: 577-589.
40. Schwer, B., North, B.J., Frye, R.A., Ott, M., and Verdin, E. (2002) The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J Cell Biol 158: 647-657.
41. Schwer, B., Bunkenborg, J., Verdin, R.O., Andersen, J.S., and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci USA 103: 10224-10229.
42. Singer, M.S., and Gottschling, D.E. (1994) TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science 266: 404-409.
43. +-dependent protein deacetylase activity in the Sir2 protein family. Proc Natl Acad Sci USA 97: 6658-6663.
44. Starai, V.J., Celic, I., Cole, R.N., Boeke, J.D., and Escalante-Semerena, J.C. (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298: 2390-2392.
45. Tanner, K.G., Landry, J., Sternglanz, R., and Denu, J.M. (2000) Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc Natl Acad Sci USA 97: 14178-14182.
46. Tsang, A.W., and Escalante-Semerena, J.C. (1998) CobB, a new member of the SIR2 family of eucaryotic regulatory proteins, is required to compensate for the lack of nicotinate mononucleotide: 5,6-dimethylbenzimidazole phosphoribosyltransferase activity in cobT mutants during cobalamin biosynthesis in Salmonella typhimurium LT2. J Biol Chem 273: 31788-31794.
47. Tsukamoto, Y., Kato, J., and Ikeda, H. (1997) Silencing factors participate in DNA repair and recombination in Saccharomyces cerevisiae. Nature 388: 900-903.
48. Vaziri, H., Dessain, S.K., Ng Eaton, E., Imai, S.I., Frye, R.A., Pandita, T.K., et al. (2001) hSIR2 (SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159.
49. Vergnes, B., Sereno, D., Tavares, J., Cordeiro-da-Silva, A., Vanhille, L., et al. (2005) Targeted disruption of cytosolic SIR2 deacetylase discloses its essential role in Leishmania survival and proliferation. Gene 363: 85-96.
50. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99: 89-101.
51. Zemzoumi, K., Sereno, D., Francois, C., Guilvard, E., Lemesre, J.L., and Ouaissi, A. (1998) Leishmania major: cell type dependent distribution of a 43 kDa antigen related to silent information regulatory-2 protein family. Biol Cell 90: 239-245.