Toxoplasma histone acetylation remodelers as novel drug targets

Expert Review of Anti-Infective Therapy

Volumn 10, Issue 10, 2012, Pages 1189-1201

  Vanagas, Laura ^a   Jeffers, Victoria ^b   Bogado, Silvina S ^a   Dalmasso, Maria C ^a   Sullivan, William J ^b   Angel, Sergio O ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

acetylation; HATs; HDACi; HDACs; histone; therapy; Toxoplasma gondii

Indexed keywords

6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; ANACARDIC ACID; APICIDIN; AZELAICBISHYDROXAMIC ACID; BUTYRIC ACID; CURCUMIN; ENZYME INHIBITOR; FR 235222; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE INHIBITOR; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; MC 1626; NICOTINAMIDE; SIRTINOL; SUBEROHYDROXAMIC ACID; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

DNA REPAIR; DRUG MECHANISM; DRUG TARGETING; ENZYME INHIBITION; GENE EXPRESSION; GENE REPLICATION; HISTONE ACETYLATION; HUMAN; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; REVIEW; TOXOPLASMA GONDII; UBIQUITINATION;

EID: 84870617451     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.12.100     Document Type: Review

References (110)

1. Elmore SA, Jones JL, Conrad PA, Patton S, Lindsay DS, Dubey JP. Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends Parasitol. 26 (4), 190-196 (2010).
2. Su C, Evans D, Cole RH, Kissinger JC, Ajioka JW, Sibley LD. Recent expansion of Toxoplasma through enhanced oral transmission. Science 299 (5605), 414-416 (2003).
3. Isaac-Renton J, Bowie WR, King A et al. Detection of Toxoplasma gondii oocysts in drinking water. Appl. Environ. Microbiol. 64 (6), 2278-2280 (1998).
4. Choi WY, Nam HW, Kwak NH et al. Foodborne outbreaks of human toxoplasmosis. J. Infect. Dis. 175 (5), 1280-1282 (1997).
5. Carlier Y, Truyens C, Deloron P, Peyron F. Congenital parasitic infections: a review. Acta Trop. 121 (2), 55-70 (2012).
6. Brynska A, Tomaszewicz-Libudzic E, Wolanczyk T. Obsessive-compulsive disorder and acquired toxoplasmosis in two children. Eur. Child Adolesc. Psychiatry 10 (3), 200-204 (2001).
7. Miman O, Mutlu EA, Ozcan O, Atambay M, Karlidag R, Unal S. Is there any role of Toxoplasma gondii in the etiology of obsessive-compulsive disorder? Psychiatry Res. 177 (1-2), 263-265 (2010).
8. Yolken RH, Dickerson FB, Fuller Torrey E. Toxoplasma and schizophrenia. Parasite Immunol. 31 (11), 706-715 (2009).
9. Vittecoq M, Elguero E, Lafferty KD et al. Brain cancer mortality rates increase with Toxoplasma gondii seroprevalence in France. Infect. Genet. Evol. 12 (2), 496-498 (2012).
10. Luft BJ, Remington JS. Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15 (2), 211-222 (1992).
11. Baatz H, Mirshahi A, Puchta J, Gümbel H, Hattenbach LO. Reactivation of toxoplasma retinochoroiditis under atovaquone therapy in an immunocompetent patient. Ocul. Immunol. Infl amm. 14 (3), 185-187 (2006).
12. Petersen E. Prevention and treatment of congenital toxoplasmosis. Expert Rev. Anti. Infect. Ther. 5 (2), 285-293 (2007).
13. Dannemann B, McCutchan JA, Israelski D et al. Treatment of toxoplasmic encephalitis in patients with AIDS. A randomized trial comparing pyrimethamine plus clindamycin to pyrimethamine plus sulfadiazine. The California Collaborative Treatment Group. Ann. Intern. Med. 116 (1), 33-43 (1992).
14. Weiss LM, Kim K. The development and biology of bradyzoites of Toxoplasma gondii. Front. Biosci. 5, D391-D405 (2000).
15. Rodriguez JB, Szajnman SH. New antibacterials for the treatment of toxoplasmosis; a patent review. Expert Opin. Ther. Pat. 22 (3), 311-333 (2012).
16. Sullivan WJ Jr, Jeffers V. Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol. Rev. 36 (3), 717-733 (2012).
17. Sullivan WJ Jr, Hakimi MA. Histone mediated gene activation in Toxoplasma gondii. Mol. Biochem. Parasitol. 148 (2), 109-116 (2006).
18. Dalmasso MC, Sullivan WJ Jr, Angel SO. Canonical and variant histones of protozoan parasites. Front Biosci. 17 2086-2105 (2012)
19. Kamakaka RT Biggins S Histone variants: deviants? Genes Dev. 19(3) 295-310 (2005)
20. Yuan G Zhu B Histone variants and epigenetic inheritance. Biochim. Biophys. Acta. 1819(3-4) 222-229 (2012)
21. Malik HS Henikoff S Phylogenomics of the nucleosome. Nat. Struct. Biol. 10(11) 882-891 (2003)
22. Dalmasso MC Echeverria PC Zappia MP Hellman U Dubremetz JF Angel SO Toxoplasma gondii has two lineages of histones 2b (H2B) with different expression profiles. Mol. Biochem. Parasitol. 148(1) 103-107 (2006)
23. Dalmasso MC Onyango DO Naguleswaran A Sullivan WJ Jr Angel SO Toxoplasma H2A variants reveal novel insights into nucleosome composition and functions for this histone family. J. Mol. Biol. 392(1) 33-47 (2009)
24. Aul RB Oko RJ The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during sper m io genesis. Dev. Biol. 239(2) 376-387 (2001)
25. Churikov D Siino J Svetlova M et al. Novel human testis-specifi c histone H2B encoded by the interrupted gene on the X chromosome. Genomics 84(4) 745-756 (2004)
26. Churikov D Zalenskaya I A Zalensky AO Male germline-specifi c histones in mouse and man. Cytogenet. Genome Res. 105(2-4) 203-214 (2004)
27. Zalensky AO Siino JS Gineitis AA et al. Human testis/sperm-specifi c histone H2B (hTSH2B). Molecular cloning and characterization. J. Biol. Chem. 277(45) 43474-43480 (2002)
28. Alsford S Horn D Trypanosomatid histones. Mol. Microbiol. 53(2) 365-372 (2004)
29. Miao J Fan Q Cui L Li J Li J Cui L The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation. Gene 369 53-65 (2006)
30. Lowell JE Kaiser F Janzen CJ Cross GA Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei. J. Cell. Sci. 118(Pt24) 5721-5730 (2005)
31. Trelle MB Salcedo-Amaya AM Cohen AM Stunnenberg HG Jensen ON Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J. Proteome Res. 8(7) 3439-3450 (2009)
32. Jeffers V Sullivan WJ Jr Lysine acetylation is widespread on proteins of diverse function and localization in the protozoan parasite Toxoplasma gondii. Eukaryotic Cell 11(6) 735-742 (2012)
33. Basu A Rose KL Zhang J et al. Proteome-wide prediction of acetylation substrates. Proc. Natl. Acad. Sci. U.S.A. 106(33) 13785-13790 (2009)
34. Choudhary C Kumar C Gnad F et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 325(5942) 834-840 (2009)
35. Feng Y Wang J Asher S et al. Histone H4 acetylation differentially modulates arginine methylation by an in Cis mechanism J. Biol. Chem. 286(23) 20323-20334 (2011)
36. Kouzarides T Chromatin modif cations and their function. Cell 128(4) 693-705 (2007)
37. Strahl BD Allis CD The language of covalent histone modifications Nature 403(6765) 41-45 (2000)
38. Bannister AJ Kouzarides T Regulation of chromatin by histone modifications Cell Res. 21(3) 381-395 (2011)
39. Jenuwein T Allis CD Translating the histone code. Science 293(5532) 1074-1080 (2001)
40. Cheung P Allis CD Sassone-Corsi P Signaling to chromatin through histone modifications Cell 103(2) 263-271 (2000)
41. Lee KK Workman JL Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell Biol 8(4) 284-295 (2007)
42. Carrozza MJ Utley RT Workman JL Côté J The diverse functions of histone acetyltransferase complexes. Trends Genet. 19(6) 321-329 (2003)
43. Sterner DE Berger SL Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64(2) 435-459 (2000)
44. Campos EI Fillingham J Li G et al. The program for processing newly synthesized histones H3.1 and H4. Nat. Struct. Mol Biol. 17(11) 1343-1351 (2010)
45. Gregoretti IV Lee YM Goodson HV Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol 338(1) 17-31 (2004)
46. Carey N La Thangue NB Histone deacetylase inhibitors: gathering pace. Curr. Opin. Pharmacol. 6(4) 369-375 (2006)
47. Xu K Dai XL Huang HC Jiang ZF Targeting HDACs: a promising therapy for Alzheimer's disease. Oxid. Med. Cell Longev. 2011 143269 (2011)
48. Rider SD Jr Zhu G An apicomplexan ankyrin-repeat histone deacetylase with relatives in photosynthetic eukaryotes. Int. J. Parasitol. 39(7) 747-754 (2009)
49. Michishita E Park JY Burneskis JM Barrett JC Horikawa I Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell 16(10) 4623-4635 (2005)
50. Guarente L Sir2 links chromatin silencing metabolism, and aging. Genes Dev. 14(9) 1021-1026 (2000)
51. Copeland RA Solomon ME Richon VM Protein methyl transferases as a target class for drug discovery. Nat. Rev. Drug Discov. 8(9) 724-732 (2009)
52. Chung D Histone modif cation: the 'next wave' in cancer therapeutics. Trends Mol Med. 8(4 Suppl) S10-S11 (2002)
53. Kristeleit R Stimson L Workman P Aherne W Histone modif cation enzymes: novel targets for cancer drugs. Expert Opin. Emerg. Drugs 9(1) 135-154 (2004)
54. Wigle TJ Promoting illiteracy in epigenetics: an emerging therapeutic strategy. Curr. Chem. Genomics 5 (Suppl 1) 48-50 (2011)
55. Grant S Easley C Kirkpatrick P Vorinostat Nat. Rev. Drug Discov. 6(1) 21-22 (2007)
56. Rangwala S Zhang C Duvic M HDAC inhibitors for the treatment of cutaneous T-cell lymphomas Future Med. Chem. 4(4) 471-486 (2012)
57. Frew AJ Johnstone RW Bolden JE Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett. 280(2) 125-133 (2009)
58. Xargay-Torrent S López-Guerra M Saborit-Villarroya I et al. Vorinostat-induced apoptosis in mantle cell lymphoma is mediated by acetylation of proapoptotic BH3-only gene promoters. Clin. Cancer Res. 17(12) 3956-3968 (2011)
59. Noh JH Jung KH Kim JK et al. Aberrant regulation of HDAC2 mediates proliferation of hepatocellular carcinoma cells by deregulating expression of G1/S cell cycle proteins. PLoS ONE6(11) e28103 (2011)
60. Dixon SE Stilger KL Elias EV Naguleswaran A Sullivan WJ Jr A decade of epigenetic research in Toxoplasma gondii. Mol. Biochem. Parasitol. 173(1) 1-9 (2010)
61. Jammallo L Eidell K Davis PH et al. An insertional trap for conditional gene expression in Toxoplasma gondii: identifi cation of TAF250 as an essential gene. Mol. Biochem. Parasitol. 175(2) 133-143 (2011)
62. Bhatti MM Livingston M Mullapudi N Sullivan WJ Jr Pair of unusual GCN5 histone acetyltransferases and ADA2 homologues in the protozoan parasite Toxoplasma gondii. Eukaryotic Cell 5(1) 62-76 (2006)
63. Saksouk N Bhatti MM Kieffer S et al Histone-modifying complexes regulate gene expression pertinent to the differentiation of the protozoan parasite Toxoplasma gondii. Mol. Cell. Biol. 25(23) 10301-10314 (2005)
64. Daujat S Bauer UM Shah V Turner B Berger S Kouzarides T Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr. Biol. 12(24) 2090-2097 (2002)
65. Naguleswaran A Elias EV McClintick J Edenberg HJ Sullivan WJ Jr Toxoplasma gondii lysine acetyltransferase GCN5-A functions in the cellular response to alkaline stress and expression of cyst genes. PLoS Pathog 6(12) e1001232 (2010)
66. Fan Q An L Cui L PfADA2 a Plasmodium falciparum homologue of the transcriptional coactivator ADA2 and its in vivo association with the histone acetyltransferase PfGCN5. Gene 336(2) 251-261 (2004)
67. LaCount DJ Vignali M Chettier R et al. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438(7064) 103-107 (2005)
68. Bhatti MM Sullivan WJ Jr Histone acetylase GCN5 enters the nucleus via im por tin-alpha in protozoan parasite Toxoplasma gondii. J. Biol. Chem. 280(7) 5902-5908 (2005)
69. Dixon SE Bhatti MM Uversky VN Dunker AK Sullivan WJ Jr Regions of intrinsic disorder help identify a novel nuclear localization signal in Toxoplasma gondii histone acetyltransferase TgGCN5-B. Mol. Biochem. Parasitol 175(2) 192-195 (2011)
70. Smith AT Tucker-S am aras SD Fairlamb AH Sullivan WJ Jr MYST family histone acetyltransferases in the protozoan parasite Toxoplasma gondii. Eukaryotic Cell 4(12) 2057-2065 (2005)
71. Vonlaufen N Naguleswaran A Coppens I Sullivan WJ Jr MYST family lysine acetyltransferase facilitates ataxia telangiectasia mutated (ATM) kinase-mediated DNA damage response in Toxoplasma gondii. J. Biol. Chem. 285(15) 11154-11161 (2010)
72. Freitas-Junior LH Hernandez-Rivas R Ralph SA et al. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121(1) 25-36 (2005)
73. Duraisingh MT Voss TS Marty AJ et al Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121(1) 13-24 (2005)
74. Andrews KT Haque A Jones MK HDAC inhibitors in parasitic diseases. Immunol Cell Biol. 90(1) 66-77 (2012)
75. Tonkin CJ Carret CK Duraisingh MT et al. Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol. 7(4) e84 (2009)
76. Chakrabarty SP Saikumari YK Bopanna MP Balaram H Biochemical characterization of Plasmodium falciparum Sir2, a NAD +-dependent deacetylase. Mol Biochem. Parasitol. 158(2) 139-151 (2008)
77. Merrick CJ Duraisingh MT Plasmodium falciparum Sir2: an unusual sirtuin with dual histone deacetylase and ADP-ribosyltransferase activity Eukaryotic Cell 6(11) 2081-2091 (2007)
78. Braun L Cannella D Ortet P et al. A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog 6(5) e1000920 (2010)
79. Painter HJ Campbell TL Llin ás M The Apicomplexan AP2 family: integral factors regulating Plasmodium development Mol. Biochem. Parasitol. 176(1) 1-7 (2011)
80. Bougdour A Braun L Cannella D Hakimi MA Chromatin modif cations: implications in the regulation of gene expression in Toxoplasma gondii. Cell. Microbiol. 12(4) 413-423 (2010)
81. Matzke M Kanno T Daxinger L Huettel B Matzke AJ RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21(3) 367-376 (2009)
82. Verdel A Moazed D RNAi-directed assembly of heterochromatin in fi ssion yeast FEBS Lett. 579(26) 5872-5878 (2005)
83. Rooney PJ Neal LM Knoll LJ Involvement of a Toxoplasma gondii chromatin remodeling complex ortholog in developmental regulation. PLoS ONE6(5) e19570 (2011)
84. Boyle JP Saeij JP Cleary MD Boothroyd JC Analysis of gene expression during development: lessons from the Apicomplexa Microbes Infect. 8(6) 1623-1630 (2006)
85. Gissot M Kelly KA Ajioka JW Greally JM Kim K Epigenomic modif cations predict active promoters and gene structure in Toxoplasma gondii. PLoS Pathog. 3(6) e77 (2007)
86. Behnke MS Radke JB Smith AT Sullivan WJ Jr White MW The transcription of bradyzoite genes in Toxoplasma gondii is controlled by autonomous promoter elements. Mol. Microbiol. 68(6) 1502-1518 (2008)
87. Patil V Guerrant W Chen PC et al Antimalarial and antileishmanial activities of histone deacetylase inhibitors with triazole-linked cap group. Bioorg Med. Chem. 18(1) 415-425 (2010)
88. Darkin-Rattray SJ Gurnett AM Myers RW et al. Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase Proc. Natl. Acad. Sci. U. S.A. 93(23) 13143-13147 (1996)
89. Strobl JS Cassell M Mitchell SM Reilly CM Lindsay DS Scriptaid and suberoylanilide hydroxamic acid are histone deacetylase inhibitors with potent anti-Toxoplasma gondii activity in vitro. J. Parasitol. 93(3) 694-700 (2007)
90. Bougdour A Maubon D Baldacci P et al Drug inhibition of HDAC3 and epigenetic control of differentiation in Apicomplexa parasites J. Exp. Med. 206(4) 953-966 (2009)
91. Sonda S Morf L Bottova I et al. Epigenetic mechanisms regulate stage differentiation in the minimized protozoan Giardia lamblia Mol. Microbiol. 76(1) 48-67 (2010)
92. Jerome ME Radke JR Bohne W Roos DS White MW Toxoplasma gondii bradyzoites form spontaneously during sporozoite-initiated development Infect. Immun. 66(10) 4838-4844 (1998)
93. Maubon D Bougdour A Wong YS et al. Activity of the histone deacetylase inhibitor FR235222 on Toxoplasma gondii: inhibition of stage conversion of the parasite cyst form and study of new derivative compounds Antimicrob. Agents Chemother. 54(11) 4843-4850 (2010)
94. Furdas SD Kannan S Sippl W Jung M Small molecule inhibitors of histone acetyltransferases as epigenetic tools and drug candidates. Arch. Pharm. (Weinheim) 345(1) 7-21 (2012)
95. Smith AT Livingston MR Mai A Filetici P Queener SF Sullivan WJ Jr Quinoline derivative MC1626, a putative GCN5 histone acetyl transferase (HAT) inhibitor, exhibits HAT-independent activity against Toxoplasma gondii. Antimicrob. Agents Chemother. 51(3), 1109-1111 (2007).
96. Cui L Miao J Cui L Cytotoxic effect of curcumin on malaria parasite Plasmodium falciparum: inhibition of histone acetylation and generation of reactive oxygen species Antimicrob. Agents Chemother. 51(2) 488-494 (2007)
97. Cui L Miao J Furuya T et al. Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development Eukaryotic Cell7(7) 1200-1210 (2008)
98. Zhao S, Xu W, Jiang W, et al. Regulation of cellular metabolism by protein lysine acetylation Science 327 (5968) 1000-1004 (2010)
99. Jones-Brando L, Torrey EF, Yolken R Drugs used in the treatment of schizophrenia and bipolar disorder inhibit the replication of Toxoplasmagondii Schizophr. Res. 62 (3) 237-244 (2003)
100. Azzi A, Cosseau C, Grunau C. Schistosoma mansoni: developmental arrest of miracidia treated with histone deacetylase inhibitors. Exp. Parasitol. 121 (3) 288-291 (2009)
101. Dubois F, Caby S, Oger F et al. Histone deacetylase inhibitors induce apoptosis, histone hyperacetylation and up-regulation of gene transcription in Schistosoma mansoni. Mol. Biochem. Parasitol. 168 (1), 7-15 (2009).
102. Colletti SL, Myers RW, Darkin-Rattray SJ et al. Broad spectrum antiprotozoal agents that inhibit histone deacetylase: structureactivity relationships of apicidin. Part 1. Bioorg. Med. Chem. Lett. 11 (2), 107-111 (2001).
103. Colletti SL, Myers RW, Darkin-Rattray SJ et al. Broad spectrum antiprotozoal agents that inhibit histone deacetylase: structureactivity relationships of apicidin. Part 2. Bioorg. Med. Chem. Lett. 11 (2), 113-117 (2001).
104. Chaal BK, Gupta AP, Wastuwidyaningtyas BD, Luah YH, Bozdech Z. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog. 6 (1), e1000737 (2010).
105. Andrews KT, Walduck A, Kelso MJ, Fairlie DP, Saul A, Parsons PG. Anti-malarial effect of histone deacetylation inhibitors and mammalian tumour cytodifferentiating agents. Int. J. Parasitol. 30 (6), 761-768 (2000).
106. Andrews KT, Tran TN, Lucke AJ et al. Potent antimalarial activity of histone deacetylase inhibitor analogues. Antimicrob. Agents Chemother. 52 (4), 1454-1461 (2008).
107. Prusty D, Mehra P, Srivastava S et al. Nicotinamide inhibits Plasmodium falciparum Sir2 activity in vitro and parasite growth. FEMS Microbiol. Lett. 282 (2), 266-272 (2008).
108. Vergnes B, Vanhille L, Ouaissi A, Sereno D. Stage-specifi c antileishmanial activity of an inhibitor of SIR2 histone deacetylase. Acta Trop. 94 (2), 107-115 (2005).
109. Singh N, Misra K. Computational screening of molecular targets in Plasmodium for novel non resistant anti-malarial drugs. Bioinformation 3 (6), 255-262 (2009).
110. Martinelli A, Rodrigues LA, Cravo P. Plasmodium chabaudi : effi cacy of artemisinin + curcumin combination treatment on a clone selected for artemisinin resistance in mice. Exp. Parasitol. 119 (2), 304-307 (2008).