Sirtuins of parasitic protozoa: In search of function(s)

Molecular and Biochemical Parasitology

Volumn 185, Issue 2, 2012, Pages 71-88

  Religa, Agnieszka A ^a   Waters, Andrew P ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Antigenic variation; Gene regulation; Leishmania; Parasite; Plasmodium; sir2

Indexed keywords

ANTIPARASITIC AGENT; SIRTUIN; SIRTUIN 2; SIRTUIN 2A; SIRTUIN 2B; SIRTUIN ACTIVATOR; SIRTUIN INHIBITOR; UNCLASSIFIED DRUG;

APICOMPLEXA; BABESIA BOVIS; CRYPTOSPORIDIUM; EIMERIA TENELLA; GIARDIA LAMBLIA; IC 50; KINETOPLASTIDA; LEISHMANIA; MICROBIAL DIVERSITY; NEOSPORA CANINUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; THEILERIA; TOXOPLASMA; TRICHOMONAS VAGINALIS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

ANIMALS; APICOMPLEXA; HUMANS; PHYLOGENY; PROTOZOAN PROTEINS; SIRTUIN 2; SIRTUINS;

APICOMPLEXA; PLASMODIUM (APICOMPLEXA); PROTOZOA; TRYPANOSOMA;

EID: 84866891556     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2012.08.003     Document Type: Review

References (189)

1. A.J. Klar, S. Fogel, and K. Macleod MAR1 - a regulator of the HMa and HMalpha loci in Saccharomyces cerevisiae Genetics 93 1979 37 50
2. J. Rine, J.N. Strathern, J.B. Hicks, and I. Herskowitz A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci Genetics 93 1979 877 901
3. D. Herranz, M. Munoz-Martin, M. Canamero, F. Mulero, B. Martinez-Pastor, and O. Fernandez-Capetillo Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer Nature Communications 1 2010 3
4. M.C. Haigis, and D.A. Sinclair Mammalian sirtuins: biological insights and disease relevance Annual Review of Pathology 5 2010 253 295
5. X. Li, and N. Kazgan Mammalian sirtuins and energy metabolism International Journal of Biological Sciences 7 2011 575 587
6. A. Satoh, L. Stein, and S. Imai The role of mammalian sirtuins in the regulation of metabolism, aging, and longevity Handbook of Experimental Pharmacology 206 2011 125 162
7. M. Kaeberlein Lessons on longevity from budding yeast Nature 464 2010 513 519
8. N. li-Youcef, M. Lagouge, S. Froelich, C. Koehl, K. Schoonjans, and J. Auwerx Sirtuins: the 'magnificent seven', function, metabolism and longevity Annals of Medicine 39 2007 335 345
9. R. Rajendran, R. Garva, M. Krstic-Demonacos, and C. Demonacos Sirtuins: molecular traffic lights in the crossroad of oxidative stress, chromatin remodeling, and transcription Journal of Biomedicine and Biotechnology 2011 2011 368276
10. R.A. Frye Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins Biochemical and Biophysical Research Communications 273 2000 793 798
11. S. Greiss, and A. Gartner Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation Molecules and Cells 28 2009 407 415
12. C.J. Tonkin, C.K. Carret, M.T. Duraisingh, T.S. Voss, S.A. Ralph, and M. Hommel Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum PLoS Biology 7 2009 e84
13. C.J. Merrick, and M.T. Duraisingh Plasmodium falciparum Sir2: an unusual sirtuin with dual histone deacetylase and ADP-ribosyltransferase activity Eukaryotic Cell 6 2007 2081 2091
14. J.M. Carlton, R.P. Hirt, J.C. Silva, A.L. Delcher, M. Schatz, and Q. Zhao Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis Science 315 2007 207 212
15. B.D. Sanders, B. Jackson, and R. Marmorstein Structural basis for sirtuin function: what we know and what we don't Biochimica et Biophysica Acta 1804 2010 1604 1616
16. +-dependent histone deacetylase SIRT1 Journal of Biological Chemistry 282 2007 6823 6832
17. S.P. Chakrabarty, and H. Balaram Reversible binding of zinc in Plasmodium falciparum Sir2: structure and activity of the apoenzyme Biochimica et Biophysica Acta 1804 2010 1743 1750
18. A.W. Tsang, and J.C. Escalante-Semerena 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 Journal of Biological Chemistry 273 1998 31788 31794
19. R.A. Frye Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity Biochemical and Biophysical Research Communications 260 1999 273 279
20. J.C. Tanny, G.J. Dowd, J. Huang, H. Hilz, and D. Moazed An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing Cell 99 1999 735 745
21. S. Imai, C.M. Armstrong, M. Kaeberlein, and L. Guarente Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase Nature 403 2000 795 800
22. K. Fahie, P. Hu, S. Swatkoski, Y. Zhang, and C. Wolberger Side chain specificity of ADP-ribosylation by a sirtuin FEBS Journal 276 2009 7159 7176
23. M.C. Haigis, R. Mostoslavsky, K.M. Haigis, K. Fahie, D.C. Christodoulou, and A.J. Murphy SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells Cell 126 2006 941 954
24. A. Herrero-Yraola, S.M. Bakhit, P. Franke, C. Weise, M. Schweiger, and D. Jorcke Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria EMBO Journal 20 2001 2404 2412
25. T.M. Kowieski, S. Lee, and J.M. Denu Acetylation-dependent ADP-ribosylation by Trypanosoma brucei Sir2 Journal of Biological Chemistry 283 2008 5317 5326
26. J. Du, H. Jiang, and H. Lin Investigating the ADP-ribosyltransferase activity of sirtuins with NAD analogues and 32P-NAD Biochemistry 48 2009 2878 2890
27. K.G. Tanner, J. Landry, R. Sternglanz, and J.M. Denu Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose Proceedings of the National Academy of Sciences of the United States of America 97 2000 14178 14182
28. G. Liszt, E. Ford, M. Kurtev, and L. Guarente Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyl transferase Journal of Biological Chemistry 280 2005 21313 21320
29. J. Du, Y. Zhou, X. Su, J.J. Yu, S. Khan, and H. Jiang Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase Science 334 2011 806 809
30. C. Peng, Z. Lu, Z. Xie, Z. Cheng, Y. Chen, and M. Tan The first identification of lysine malonylation substrates and its regulatory enzyme Molecular and Cellular Proteomics 10 2011 M111
31. Z. Zhang, M. Tan, Z. Xie, L. Dai, Y. Chen, and Y. Zhao Identification of lysine succinylation as a new post-translational modification Nature Chemical Biology 7 2011 58 63
32. T. Nakagawa, D.J. Lomb, M.C. Haigis, and L. Guarente SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle Cell 137 2009 560 570
33. J. Landry, J.T. Slama, and R. Sternglanz Role of NAD(+) in the deacetylase activity of the SIR2-like proteins Biochemical and Biophysical Research Communications 278 2000 685 690
34. S. Michan, and D. Sinclair Sirtuins in mammals: insights into their biological function Biochemical Journal 404 2007 1 13
35. G. Donmez, D. Wang, D.E. Cohen, and L. Guarente SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10 Cell 142 2010 320 332
36. W. Fan, and J. Luo SIRT1 regulates UV-induced DNA repair through deacetylating XPA Molecular Cell 39 2010 247 258
37. E.F. Joyce, and K.S. McKim Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis PLoS Genetics 2010 6
38. S. Laskar, M.K. Bhattacharyya, R. Shankar, and S. Bhattacharyya HSP90 controls SIR2 mediated gene silencing PLoS ONE 6 2011 e23406
39. J.H. Lim, Y.M. Lee, Y.S. Chun, J. Chen, J.E. Kim, and J.W. Park Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha Molecular Cell 38 2010 864 878
40. I. Mattagajasingh, C.S. Kim, A. Naqvi, T. Yamamori, T.A. Hoffman, and S.B. Jung SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase Proceedings of the National Academy of Sciences of the United States of America 104 2007 14855 14860
41. S.H. Millson, A.W. Truman, V. King, C. Prodromou, L.H. Pearl, and P.W. Piper A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p) Eukaryotic Cell 4 2005 849 860
42. F. Wang, and Q. Tong SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1s repressive interaction with PPARgamma Molecular Biology of the Cell 20 2009 801 808
43. A. Vaquero, and D. Reinberg Calorie restriction and the exercise of chromatin Genes and Development 23 2009 1849 1869
44. S. Ghosh, S. George, U. Roy, D. Ramachandran, and U. Kolthur-Seetharam NAD: a master regulator of transcription Biochimica et Biophysica Acta 1799 2010 681 693
45. M. Naimi, C. Arous, and O.E. Van Energetic cell sensors: a key to metabolic homeostasis Trends in Endocrinology & Metabolism 21 2010 75 82
46. P.A. Mieczkowski, M. Dominska, M.J. Buck, J.D. Lieb, and T.D. Petes Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae Proceedings of the National Academy of Sciences of the United States of America 104 2007 3955 3960
47. Z. Mao, C. Hine, X. Tian, M. Van Meter, M. Au, and A. Vaidya SIRT6 promotes DNA repair under stress by activating PARP1 Science 332 2011 1443 1446
48. P. Oberdoerffer, S. Michan, M. McVay, R. Mostoslavsky, J. Vann, and S.K. Park SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging Cell 135 2008 907 918
49. H. Aguilaniu, L. Gustafsson, M. Rigoulet, and T. Nystrom Asymmetric inheritance of oxidatively damaged proteins during cytokinesis Science 299 2003 1751 1753
50. N. Erjavec, and T. Nystrom Sir2p-dependent protein segregation gives rise to a superior reactive oxygen species management in the progeny of Saccharomyces cerevisiae Proceedings of the National Academy of Sciences of the United States of America 104 2007 10877 10881
51. N. Erjavec, M. Cvijovic, E. Klipp, and T. Nystrom Selective benefits of damage partitioning in unicellular systems and its effects on aging Proceedings of the National Academy of Sciences of the United States of America 105 2008 18764 18769
52. A.B. Lindner, R. Madden, A. Demarez, E.J. Stewart, and F. Taddei Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation Proceedings of the National Academy of Sciences of the United States of America 105 2008 3076 3081
53. B. Liu, L. Larsson, A. Caballero, X. Hao, D. Oling, and J. Grantham The polarisome is required for segregation and retrograde transport of protein aggregates Cell 140 2010 257 267
54. S. Lee, L. Tong, and J.M. Denu Quantification of endogenous sirtuin metabolite O-acetyl-ADP-ribose Analytical Biochemistry 383 2008 174 179
55. G. Kustatscher, M. Hothorn, C. Pugieux, K. Scheffzek, and A.G. Ladurner Splicing regulates NAD metabolite binding to histone macroH2A Nature Structural & Molecular Biology 12 2005 624 625
56. O. Grubisha, L.A. Rafty, C.L. Takanishi, X. Xu, L. Tong, and A.L. Perraud Metabolite of SIR2 reaction modulates TRPM2 ion channel Journal of Biological Chemistry 281 2006 14057 14065
57. G.G. Liou, J.C. Tanny, R.G. Kruger, T. Walz, and D. Moazed Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation Cell 121 2005 515 527
58. O.M. Aparicio, B.L. Billington, and D.E. Gottschling Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae Cell 66 1991 1279 1287
59. D. Moazed, A.D. Rudner, J. Huang, G.J. Hoppe, and J.C. Tanny A model for step-wise assembly of heterochromatin in yeast Novartis Foundation Symposium 259 2004 48 56
60. L.N. Rusche, A.L. Kirchmaier, and J. Rine The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae Annual Review of Biochemistry 72 2003 481 516
61. M. Ruault, M.A. De, I. Loiodice, and A. Taddei Clustering heterochromatin: Sir3 promotes telomere clustering independently of silencing in yeast Journal of Cell Biology 192 2011 417 431
62. G. Kyrion, K. Liu, C. Liu, and A.J. Lustig RAP1 and telomere structure regulate telomere position effects in Saccharomyces cerevisiae Genes and Development 7 1993 1146 1159
63. S.J. Boulton, and S.P. Jackson Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing EMBO Journal 17 1998 1819 1828
64. W.H. Tham, and V.A. Zakian Transcriptional silencing at Saccharomyces telomeres: implications for other organisms Oncogene 21 2002 512 521
65. J.A. Baur, W.E. Wright, and J.W. Shay Analysis of mammalian telomere position effect Methods in Molecular Biology 287 2004 121 136
66. D.E. Gottschling, O.M. Aparicio, B.L. Billington, and V.A. Zakian Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription Cell 63 1990 751 762
67. A. Ottaviani, E. Gilson, and F. Magdinier Telomeric position effect: from the yeast paradigm to human pathologies Biochimie 90 2008 93 107
68. H. Renauld, O.M. Aparicio, P.D. Zierath, B.L. Billington, S.K. Chhablani, and D.E. Gottschling Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage Genes and Development 7 1993 1133 1145
69. J.A. Baur, Y. Zou, J.W. Shay, and W.E. Wright Telomere position effect in human cells Science 292 2001 2075 2077
70. K.A. Nasmyth, K. Tatchell, B.D. Hall, C. Astell, and M. Smith A position effect in the control of transcription at yeast mating type loci Nature 289 1981 244 250
71. S. Gottlieb, and R.E. Esposito A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA Cell 56 1989 771 776
72. P. Horrocks, E. Wong, K. Russell, and R.D. Emes Control of gene expression in Plasmodium falciparum - ten years on Molecular and Biochemical Parasitology 164 2009 9 25
73. L.H. Freitas-Junior, R. Hernandez-Rivas, S.A. Ralph, D. Montiel-Condado, O.K. Ruvalcaba-Salazar, and A.P. Rojas-Meza Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites Cell 121 2005 25 36
74. M.T. Duraisingh, T.S. Voss, A.J. Marty, M.F. Duffy, R.T. Good, and J.K. Thompson Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum Cell 121 2005 13 24
75. J.M. Carlton, S.V. Angiuoli, B.B. Suh, T.W. Kooij, M. Pertea, and J.C. Silva Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii Nature 419 2002 512 519
76. A. Scherf, R. Hernandez-Rivas, P. Buffet, E. Bottius, C. Benatar, and B. Pouvelle Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum EMBO Journal 17 1998 5418 5426
77. T. Chookajorn, P. Ponsuwanna, and L. Cui Mutually exclusive var gene expression in the malaria parasite: multiple layers of regulation Trends in Parasitology 24 2008 455 461
78. K.W. Deitsch, P.A. del, and T.E. Wellems Intra-cluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum Molecular and Biochemical Parasitology 101 1999 107 116
79. R. Dzikowski, F. Li, B. Amulic, A. Eisberg, M. Frank, and S. Patel Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites EMBO Reports 8 2007 959 965
80. A.J. Marty, J.K. Thompson, M.F. Duffy, T.S. Voss, A.F. Cowman, and B.S. Crabb Evidence that Plasmodium falciparum chromosome end clusters are cross-linked by protein and are the sites of both virulence gene silencing and activation Molecular Microbiology 62 2006 72 83
81. S.A. Ralph, C. Scheidig-Benatar, and A. Scherf Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations Proceedings of the National Academy of Sciences of the United States of America 102 2005 5414 5419
82. S.M. Kraemer, S.A. Kyes, G. Aggarwal, A.L. Springer, S.O. Nelson, and Z. Christodoulou Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates BMC Genomics 8 2007 45
83. T.S. Voss, J.K. Thompson, J. Waterkeyn, I. Felger, N. Weiss, and A.F. Cowman Genomic distribution and functional characterisation of two distinct and conserved Plasmodium falciparum var gene 5' flanking sequences Molecular and Biochemical Parasitology 107 2000 103 115
84. C.J. Merrick, R. Dzikowski, H. Imamura, J. Chuang, K. Deitsch, and M.T. Duraisingh The effect of Plasmodium falciparum Sir2a histone deacetylase on clonal and longitudinal variation in expression of the var family of virulence genes International Journal for Parasitology 40 2010 35 43
85. C.J. Merrick, C. Huttenhower, C. Buckee, A. Amambua-Ngwa, N. Gomez-Escobar, and M. Walther Epigenetic dysregulation of virulence gene expression in severe Plasmodium falciparum malaria Journal of Infectious Diseases 205 2012 1593 1600
86. A.T. Jensen, P. Magistrado, S. Sharp, L. Joergensen, T. Lavstsen, and A. Chiucchiuini Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes Journal of Experimental Medicine 199 2004 1179 1190
87. M. Kaestli, I.A. Cockburn, A. Cortes, K. Baea, J.A. Rowe, and H.P. Beck Virulence of malaria is associated with differential expression of Plasmodium falciparum var gene subgroups in a case-control study Journal of Infectious Diseases 193 2006 1567 1574
88. H.M. Kyriacou, G.N. Stone, R.J. Challis, A. Raza, K.E. Lyke, and M.A. Thera Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia Molecular and Biochemical Parasitology 150 2006 211 218
89. M. Rottmann, T. Lavstsen, J.P. Mugasa, M. Kaestli, A.T. Jensen, and D. Muller Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children Infection and Immunity 74 2006 3904 3911
90. G.M. Warimwe, T.M. Keane, G. Fegan, J.N. Musyoki, C.R. Newton, and A. Pain Plasmodium falciparum var gene expression is modified by host immunity Proceedings of the National Academy of Sciences of the United States of America 106 2009 21801 21806
91. R.M. Anderson, R.M. May, and S. Gupta Non-linear phenomena in host-parasite interactions Parasitology 99 Suppl 1989 S59 S79
92. K. Dietz, G. Raddatz, and L. Molineaux Mathematical model of the first wave of Plasmodium falciparum asexual parasitemia in non-immune and vaccinated individuals American Journal of Tropical Medicine and Hygiene 75 2006 46 55
93. L. Molineaux, H.H. Diebner, M. Eichner, W.E. Collins, G.M. Jeffery, and K. Dietz Plasmodium falciparum parasitaemia described by a new mathematical model Parasitology 122 2001 379 391
94. M. Petter, C.C. Lee, T.J. Byrne, K.E. Boysen, J. Volz, and S.A. Ralph Expression of P. falciparum var genes involves exchange of the histone variant H2A.Z at the promoter PLoS Pathogens 7 2011 e1001292
95. R. Hernandez-Rivas, K. Perez-Toledo, A.M. Herrera Solorio, D.M. Delgadillo, and M. Vargas Telomeric heterochromatin in Plasmodium falciparum Journal of Biomedicine and Biotechnology 2010 2010 290501
96. L. Mancio-Silva, A.P. Rojas-Meza, M. Vargas, A. Scherf, and R. Hernandez-Rivas Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum Journal of Cell Science 121 2008 2046 2053
97. D. de Bruin, S.M. Kantrow, R.A. Liberatore, and V.A. Zakian Telomere folding is required for the stable maintenance of telomere position effects in yeast Molecular and Cellular Biology 20 2000 7991 8000
98. S. Strahl-Bolsinger, A. Hecht, K. Luo, and M. Grunstein SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast Genes and Development 11 1997 83 93
99. K. Perez-Toledo, A.P. Rojas-Meza, L. Mancio-Silva, N.A. Hernandez-Cuevas, D.M. Delgadillo, and M. Vargas Plasmodium falciparum heterochromatin protein 1 binds to tri-methylated histone 3 lysine 9 and is linked to mutually exclusive expression of var genes Nucleic Acids Research 37 2009 2596 2606
100. D.T. Pak, M. Pflumm, I. Chesnokov, D.W. Huang, R. Kellum, and J. Marr Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes Cell 91 1997 311 323
101. M.M. Shareef, C. King, M. Damaj, R. Badagu, D.W. Huang, and R. Kellum Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing Molecular Biology of the Cell 12 2001 1671 1685
102. D.W. Huang, L. Fanti, D.T. Pak, M.R. Botchan, S. Pimpinelli, and R. Kellum Distinct cytoplasmic and nuclear fractions of Drosophila heterochromatin protein 1: their phosphorylation levels and associations with origin recognition complex proteins Journal of Cell Biology 142 1998 307 318
103. M. Gotta, T. Laroche, A. Formenton, L. Maillet, H. Scherthan, and S.M. Gasser The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae Journal of Cell Biology 134 1996 1349 1363
104. A. Scherf, and D. Mattei Cloning and characterization of chromosome breakpoints of Plasmodium falciparum: breakage and new telomere formation occurs frequently and randomly in subtelomeric genes Nucleic Acids Research 20 1992 1491 1496
105. L.H. Freitas-Junior, E. Bottius, L.A. Pirrit, K.W. Deitsch, C. Scheidig, and F. Guinet Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum Nature 407 2000 1018 1022
106. N. Issar, S.A. Ralph, L. Mancio-Silva, C. Keeling, and A. Scherf Differential sub-nuclear localisation of repressive and activating histone methyl modifications in P. falciparum Microbes and Infection 11 2009 403 407
107. J.J. Lopez-Rubio, L. Mancio-Silva, and A. Scherf Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites Cell Host & Microbe 5 2009 179 190
108. +-dependent deacetylase Molecular and Biochemical Parasitology 158 2008 139 151
109. J.B. French, Y. Cen, and A.A. Sauve Plasmodium falciparum Sir2 is an NAD(+)-dependent deacetylase and an acetyllysine-dependent and acetyllysine-independent NAD(+) glycohydrolase Biochemistry 2008
110. F. Cubizolles, F. Martino, S. Perrod, and S.M. Gasser A homotrimer-heterotrimer switch in Sir2 structure differentiates rDNA and telomeric silencing Molecular Cell 21 2006 825 836
111. M. Goyal, A. Alam, M.S. Iqbal, S. Dey, S. Bindu, and C. Pal Identification and molecular characterization of an Alba-family protein from human malaria parasite Plasmodium falciparum Nucleic Acids Research 2011
112. A. Chene, S.S. Vembar, L. Riviere, J.J. Lopez-Rubio, A. Claes, and T.N. Siegel PfAlbas constitute a new eukaryotic DNA/RNA-binding protein family in malaria parasites Nucleic Acids Research 2011
113. N. Issar, E. Roux, D. Mattei, and A. Scherf Identification of a novel post-translational modification in Plasmodium falciparum: protein sumoylation in different cellular compartments Cellular Microbiology 10 2008 1999 2011
114. Y. Yang, W. Fu, J. Chen, N. Olashaw, X. Zhang, and S.V. Nicosia SIRT1 sumoylation regulates its deacetylase activity and cellular response to genotoxic stress Nature Cell Biology 9 2007 1253 1262
115. T. Sasaki, B. Maier, K.D. Koclega, M. Chruszcz, W. Gluba, and P.T. Stukenberg Phosphorylation regulates SIRT1 function PLoS ONE 3 2008 e4020
116. M.R. Hara, N. Agrawal, S.F. Kim, M.B. Cascio, M. Fujimuro, and Y. Ozeki S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding Nature Cell Biology 7 2005 665 674
117. M.D. Kornberg, N. Sen, M.R. Hara, K.R. Juluri, J.V. Nguyen, and A.M. Snowman GAPDH mediates nitrosylation of nuclear proteins Nature Cell Biology 12 2010 1094 1100
118. K.L. Olszewski, J.M. Morrisey, D. Wilinski, J.M. Burns, A.B. Vaidya, and J.D. Rabinowitz Host-parasite interactions revealed by Plasmodium falciparum metabolomics Cell Host & Microbe 5 2009 191 199
119. C.R. Zerez, E.F. Roth Jr., S. Schulman, and K.R. Tanaka Increased nicotinamide adenine dinucleotide content and synthesis in Plasmodium falciparum-infected human erythrocytes Blood 75 1990 1705 1710
120. K.L. Olszewski, M.W. Mather, J.M. Morrisey, B.A. Garcia, A.B. Vaidya, and J.D. Rabinowitz Branched tricarboxylic acid metabolism in Plasmodium falciparum Nature 466 2010 774 778
121. J.P. Daily, D. Scanfeld, N. Pochet, K. Le Roch, D. Plouffe, and M. Kamal Distinct physiological states of Plasmodium falciparum in malaria-infected patients Nature 450 2007 1091 1095
122. R. Mostoslavsky, K.F. Chua, D.B. Lombard, W.W. Pang, M.R. Fischer, and L. Gellon Genomic instability and aging-like phenotype in the absence of mammalian SIRT6 Cell 124 2006 315 329
123. A. Kaidi, B.T. Weinert, C. Choudhary, and S.P. Jackson Human SIRT6 promotes DNA end resection through CtIP deacetylation Science 329 2010 1348 1353
124. E. Michishita, R.A. McCord, L.D. Boxer, M.F. Barber, T. Hong, and O. Gozani Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6 Cell Cycle 8 2009 2664 2666
125. B. Yang, B.M. Zwaans, M. Eckersdorff, and D.B. Lombard The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability Cell Cycle 8 2009 2662 2663
126. R.I. Tennen, and K.F. Chua Chromatin regulation and genome maintenance by mammalian SIRT6 Trends in Biochemical Sciences 36 2011 39 46
127. E. Michishita, J.Y. Park, J.M. Burneskis, J.C. Barrett, and I. Horikawa Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins Molecular Biology of the Cell 16 2005 4623 4635
128. E. Ford, R. Voit, G. Liszt, C. Magin, I. Grummt, and L. Guarente Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription Genes and Development 20 2006 1075 1080
129. D.R. Allred, R.M. Cinque, T.J. Lane, and K.P. Ahrens Antigenic variation of parasite-derived antigens on the surface of Babesia bovis-infected erythrocytes Infection and Immunity 62 1994 91 98
130. R.M. O'Connor, T.J. Lane, S.E. Stroup, and D.R. Allred Characterization of a variant erythrocyte surface antigen (VESA1) expressed by Babesia bovis during antigenic variation Molecular and Biochemical Parasitology 89 1997 259 270
131. B. Al-Khedery, and D.R. Allred Antigenic variation in Babesia bovis occurs through segmental gene conversion of the ves multigene family, within a bidirectional locus of active transcription Molecular Microbiology 59 2006 402 414
132. H. Yasukawa, and K. Yagita Silent information regulator 2 proteins encoded by Cryptosporidium parasites Parasitology Research 107 2010 707 712
133. D.K. Howe, A.C. Crawford, D. Lindsay, and L.D. Sibley The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii Infection and Immunity 66 1998 5322 5328
134. E. Tabares, D. Ferguson, J. Clark, P.E. Soon, K.L. Wan, and F. Tomley Eimeria tenella sporozoites and merozoites differentially express glycosylphosphatidylinositol-anchored variant surface proteins Molecular and Biochemical Parasitology 135 2004 123 132
135. S.K. Kim, and J.C. Boothroyd Stage-specific expression of surface antigens by Toxoplasma gondii as a mechanism to facilitate parasite persistence Journal of Immunology 174 2005 8038 8048
136. Y.P. Chow, K.L. Wan, D.P. Blake, F. Tomley, and S. Nathan Immunogenic Eimeria tenella glycosylphosphatidylinositol-anchored surface antigens (SAGs) induce inflammatory responses in avian macrophages PLoS ONE 6 2011 e25233
137. J.R. Mineo, R. McLeod, D. Mack, J. Smith, I.A. Khan, and K.H. Ely Antibodies to Toxoplasma gondii major surface protein (SAG-1, P30) inhibit infection of host cells and are produced in murine intestine after peroral infection Journal of Immunology 150 1993 3951 3964
138. A. Hemphill, and B. Gottstein Identification of a major surface protein on Neospora caninum tachyzoites Parasitology Research 82 1996 497 504
139. I.D. Manger, A.B. Hehl, and J.C. Boothroyd The surface of Toxoplasma tachyzoites is dominated by a family of glycosylphosphatidylinositol-anchored antigens related to SAG1 Infection and Immunity 66 1998 2237 2244
140. Y. Nishikawa, X. Xuan, H. Nagasawa, I. Igarashi, K. Fujisaki, and H. Otsuka Monoclonal antibody inhibition of Neospora caninum tachyzoite invasion into host cells International Journal for Parasitology 30 2000 51 58
141. A. Fernandez-Garcia, V. Risco-Castillo, A. Zaballos, G. Alvarez-Garcia, and L.M. Ortega-Mora Identification and molecular cloning of the Neospora caninum SAG4 gene specifically expressed at bradyzoite stage Molecular and Biochemical Parasitology 146 2006 89 97
142. J.P. Saeij, G. Arrizabalaga, and J.C. Boothroyd A cluster of four surface antigen genes specifically expressed in bradyzoites, SAG2CDXY, plays an important role in Toxoplasma gondii persistence Infection and Immunity 76 2008 2402 2410
143. V. Risco-Castillo, V. Marugan-Hernandez, A. Fernandez-Garcia, A. Aguado-Martinez, E. Jimenez-Ruiz, and S. Rodriguez-Marco Identification of a gene cluster for cell-surface genes of the SRS superfamily in Neospora caninum and characterization of the novel SRS9 gene Parasitology 2011 1 11
144. W. Weir, T. Karagenc, M. Baird, A. Tait, and B.R. Shiels Evolution and diversity of secretome genes in the apicomplexan parasite Theileria annulata BMC Genomics 11 2010 42
145. D.A. Barnes, A. Bonnin, J.X. Huang, L. Gousset, J. Wu, and J. Gut A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion Molecular and Biochemical Parasitology 96 1998 93 110
146. A.M. Cevallos, N. Bhat, R. Verdon, D.H. Hamer, B. Stein, and S. Tzipori Mediation of Cryptosporidium parvum infection in vitro by mucin-like glycoproteins defined by a neutralizing monoclonal antibody Infection and Immunity 68 2000 5167 5175
147. G.M. Allison, K.A. Rogers, A. Borad, S. Ahmed, M.M. Karim, and A.V. Kane Antibody responses to the immunodominant Cryptosporidium gp15 antigen and gp15 polymorphisms in a case-control study of cryptosporidiosis in children in Bangladesh American Journal of Tropical Medicine and Hygiene 85 2011 97 104
148. J.D. Barry, and R. McCulloch Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite Advances in Parasitology 49 2001 1 70
149. L. Marcello, and J.D. Barry From silent genes to noisy populations-dialogue between the genotype and phenotypes of antigenic variation Journal of Eukaryotic Microbiology 54 2007 14 17
150. J.A. Garcia-Salcedo, P. Gijon, D.P. Nolan, P. Tebabi, and E. Pays A chromosomal SIR2 homologue with both histone NAD-dependent ADP- ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei EMBO Journal 22 2003 5851 5862
151. S. Alsford, T. Kawahara, C. Isamah, and D. Horn 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 63 2007 724 736
152. F. van Leeuwen, E.R. Wijsman, R. Kieft, G.A. van der Marel, J.H. van Boom, and P. Borst Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei Genes and Development 11 1997 3232 3241
153. D.K. Ekanayake, M.J. Cipriano, and R. Sabatini Telomeric co-localization of the modified base J and contingency genes in the protozoan parasite Trypanosoma cruzi Nucleic Acids Research 35 2007 6367 6377
154. A.C. Ivens, C.S. Peacock, E.A. Worthey, L. Murphy, G. Aggarwal, and M. Berriman The genome of the kinetoplastid parasite, Leishmania major Science 309 2005 436 442
155. B. Yahiaoui, A. Taibi, and A. Ouaissi A Leishmania major protein with extensive homology to silent information regulator 2 of Saccharomyces cerevisiae Gene 169 1996 115 118
156. +-dependent deacetylase and ADP-ribosyltransferase Biochemical Journal 415 2008 377 386
157. M.A. Adriano, B. Vergnes, J. Poncet, F. Mathieu-Daude, A.C. da Silva, and A. Ouaissi Proof of interaction between Leishmania SIR2RP1 deacetylase and chaperone HSP83 Parasitology Research 100 2007 811 818
158. +-dependent deacetylase Parasitology 138 2011 1245 1258
159. K. Zemzoumi, D. Sereno, C. Francois, E. Guilvard, J.L. Lemesre, and A. Ouaissi Leishmania major: cell type dependent distribution of a 43 kDa antigen related to silent information regulatory-2 protein family Biologie Cellulaire 90 1998 239 245
160. B. Vergnes, D. Sereno, N. Madjidian-Sereno, J.L. Lemesre, and A. Ouaissi Cytoplasmic SIR2 homologue overexpression promotes survival of Leishmania parasites by preventing programmed cell death Gene 296 2002 139 150
161. B. Vergnes, D. Sereno, J. Tavares, A. Cordeiro-da-Silva, L. Vanhille, and N. Madjidian-Sereno Targeted disruption of cytosolic SIR2 deacetylase discloses
162. R. Silvestre, A. Cordeiro-da-Silva, J. Tavares, D. Sereno, and A. Ouaissi Leishmania cytosolic silent information regulatory protein 2 deacetylase induces murine B-cell differentiation and in vivo production of specific antibodies Immunology 119 2006 529 540
163. R. Silvestre, A.M. Silva, A. Cordeiro-da-Silva, and A. Ouaissi The contribution of Toll-like receptor 2 to the innate recognition of a Leishmania infantum silent information regulator 2 protein Immunology 128 2009 484 499
164. M.J. de Veer, J.M. Curtis, T.M. Baldwin, J.A. DiDonato, A. Sexton, and M.J. McConville MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling European Journal of Immunology 33 2003 2822 2831
165. I. Becker, N. Salaiza, M. Aguirre, J. Delgado, N. Carrillo-Carrasco, and L.G. Kobeh Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2 Molecular and Biochemical Parasitology 130 2003 65 74
166. T.E. Nash, H.T. Lujan, M.R. Mowatt, and J.T. Conrad Variant-specific surface protein switching in Giardia lamblia Infection and Immunity 69 2001 1922 1923
167. M.R. Mowatt, A. Aggarwal, and T.E. Nash Carboxy-terminal sequence conservation among variant-specific surface proteins of Giardia lamblia Molecular and Biochemical Parasitology 49 1991 215 227
168. Y. Yang, and R.D. Adam A group of Giardia lamblia variant-specific surface protein (VSP) genes with nearly identical 5′ regions Molecular and Biochemical Parasitology 75 1995 69 74
169. R.D. Adam The Giardia lamblia genome International Journal for Parasitology 30 2000 475 484
170. Y. Yang, and R.D. Adam Allele-specific expression of a variant-specific surface protein (VSP) of Giardia lamblia Nucleic Acids Research 22 1994 2102 2108
171. T.E. Nash, J.T. Conrad, and M.R. Mowatt Giardia lamblia: identification and characterization of a variant-specific surface protein gene family Journal of Eukaryotic Microbiology 42 1995 604 609
172. L. Kulakova, S.M. Singer, J. Conrad, and T.E. Nash Epigenetic mechanisms are involved in the control of Giardia lamblia antigenic variation Molecular Microbiology 61 2006 1533 1542
173. C.G. Prucca, I. Slavin, R. Quiroga, E.V. Elias, F.D. Rivero, and A. Saura Antigenic variation in Giardia lamblia is regulated by RNA interference Nature 456 2008 750 754
174. M. Lawson, U. Uciechowska, and J. Schemies Inhibitors to understand molecular mechanisms of NAD(+)-dependent deacetylases (sirtuins) Biochimica et Biophysica Acta 1799 2010 726 739
175. D. Prusty, P. Mehra, S. Srivastava, A.V. Shivange, A. Gupta, and N. Roy Nicotinamide inhibits Plasmodium falciparum Sir2 activity in vitro and parasite growth FEMS Microbiology Letters 2008
176. S.Y. Kim, J.Y. Kim, S.H. Kim, H.J. Bae, H. Yi, and S.H. Yoon Surfactin from Bacillus subtilis displays anti-proliferative effect via apoptosis induction, cell cycle arrest and survival signaling suppression FEBS Letters 581 2007 865 871
177. B. Vergnes, L. Vanhille, A. Ouaissi, and D. Sereno Stage-specific antileishmanial activity of an inhibitor of SIR2 histone deacetylase Acta Tropica 94 2005 107 115
178. J. Tavares, A. Ouaissi, L.P. Kong Thoo, I. Loureiro, S. Kaur, and N. Roy Bisnaphthalimidopropyl derivatives as inhibitors of Leishmania SIR2 related protein 1 ChemMedChem 5 2010 140 147
179. M. Pallas, E. Verdaguer, M. Tajes, J. Gutierrez-Cuesta, and A. Camins Modulation of sirtuins: new targets for antiageing Recent Patents on CNS Drug Discovery 3 2008 61 69
180. K.T. Howitz, K.J. Bitterman, H.Y. Cohen, D.W. Lamming, S. Lavu, and J.G. Wood Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan Nature 425 2003 191 196
181. J.G. Wood, B. Rogina, S. Lavu, K. Howitz, S.L. Helfand, and M. Tatar Sirtuin activators mimic caloric restriction and delay ageing in metazoans Nature 430 2004 686 689
182. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, and A. Kalra Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 2006 337 342
183. M. Lagouge, C. Argmann, Z. Gerhart-Hines, H. Meziane, C. Lerin, and F. Daussin Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha Cell 127 2006 1109 1122
184. H.A. Tissenbaum, and L. Guarente Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans Nature 410 2001 227 230
185. B. Rogina, and S.L. Helfand Sir2 mediates longevity in the fly through a pathway related to calorie restriction Proceedings of the National Academy of Sciences of the United States of America 101 2004 15998 16003
186. M. Kaeberlein, M. McVey, and L. Guarente The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms Genes and Development 13 1999 2570 2580
187. S.J. Lin, P.A. Defossez, and L. Guarente Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae Science 289 2000 2126 2128
188. J. Huang, Q. Gan, L. Han, J. Li, H. Zhang, and Y. Sun SIRT1 overexpression antagonizes cellular senescence with activated ERK/S6k1 signaling in human diploid fibroblasts PLoS ONE 3 2008 e1710
189. S.S. Mahajan, V. Leko, J.A. Simon, and A. Bedalov Sirtuin modulators Handbook of Experimental Pharmacology 206 2011 241 255